Abstract

Background: The sagittal stratum (SS) is an important white matter (WM) structure that provides the anatomic substrate for cortico-cortical and cortico-subcortical axial interconnections necessary to overcome sensory, cognitive and motor processes. SS damage due to diseases or surgical lesions often results in significant functional losses, mainly involving serious language, visual processing, and cognitive deficits. These risks are maximized in older adults because of age-related WM degeneration.

Methods: In this comprehensive review, the research aims to synthesize research conducted on anatomy-functional roles that concern the SS, damage, and surgical outcomes. This would then separate studies that employed high neuroimaging advanced techniques, such as diffusion tensor imaging, combined with intraoperative mapping performed during awake surgery. Key attention areas will, therefore, be trajectories pointing toward lateralization of the SS tracts, age-related vulnerabilities, and the effectiveness of surgical strategies in preserving SS integrity.

Results: The review indicates that the pattern of SS damage is associated with lateralized deficits stemming from left-sided lesions, while language and vision are affected by right-sided. Older adults, already bearing significant WM degeneration, therefore, stand at a significantly greater risk of overall cognitive decline from compounding losses due to SS damage. However, advanced neuroimaging tools and refined surgical techniques have made the preservation of SS pathways much more effective, reducing long-term deficits.

Conclusion: Intraoperative preservation of SS integrity is crucial for the reduction of functional deficits and enhancement of the outcomes. Customized surgical techniques that consider tract lateralization and age-related changes are required. Further research in this area is needed.

Keywords: Cognitive functions, Neuroimaging, Sagittal stratum, Surgical outcomes, White matter tracts

INTRODUCTION

The sagittal stratum (SS) fills a very impressive crossing of neural pathways—refined in the nexus between the brain’s white matter (WM) architecture and the orchestration of many cognitive and sensory processes. Having a location on crossroads, basically, of polygon shape, the SS is formed by inferior frontal-occipital fasciculus (IFOF), Optic radiation (OR), middle longitudinal fascicle (MdlF), and other associational fibers to guarantee communication between the disparate regions of the brain’s ipsilateral hemisphere.[ 8 ] Though it is an important structure, little has been known about the SS until recent times, with many of its functional implications illuminated through advanced anatomical and imaging techniques. A better understanding of the SS is not merely an academic pursuit but a clinical imperative, given its role in key processes such as language comprehension, visual processing, and memory consolidation.

Recent research has underscored the profound clinical ramifications of SS damage, especially in neurosurgical contexts. The SS is a structure of interest and concern during surgical interventions since complex, multi-layered organization can lead to inadvertent damage with serious postoperative deficits, such as visual field cuts, language impairments, and disruptions in cognitive functions, which all argue for scrupulous surgical planning and execution.[ 21 ] The direct electrical stimulation (DES) of the SS during awake surgeries established more about its functions and showed that the stratum is implicated in more vital activities than simple sensory processing. For instance, the deficit in semantic paraphasia and other high-order linguistic functions related to surgical damage of the SS during the resection of brain tumors suggests a possible critical role for this stratum in both verbal and nonverbal human communication.[ 28 ] Furthermore, the SS itself is dynamic across the lifespan. The effects of aging-related changes on the structural integrity of the SS can be deep on its functional output; hence, the SS is one of the important targets for understanding the neurobiological substrate underlying cognitive decline in aging populations. An embryological perspective provides more about these changes, which allows for anticipating vulnerabilities that may predispose an individual to certain neurological conditions or a higher likelihood of their occurrence later in life. Essentially, the crossroad of anatomical, functional, and developmental perspectives provides an overarching framework, not only in disease but also in the whole spectrum of human development and aging, for understanding the SS.[ 8 , 21 , 28 ] The present paper seeks to delve deep into the clinical implications of SS damage and how this complex structure impacts functional outcomes in view of age-related transformations. In this respect, the current study gathers insights from anatomical dissections, clinical case studies, and embryological theories while seeking to provide an inside view into the SS with its complexities, vulnerabilities, and other key features that play a central role in the overall functioning of the brain.

METHODS

Search strategy

In this context, a critical review is given of the clinical implications due to the damage to the SS in terms of functional outcomes and considerations of age. Either published research, blended in data from case literature, was coordinated to offer views across the topic. A comprehensive search was conducted across multiple databases, including PubMed, Scopus, and Web of Science. The search strategy was developed to capture a broad range of studies about the anatomy and its functional roles, the clinical significance of SS, and different neurological conditions. The keywords used to search the literature on the SS, WM tracts, inferior frontal-occipital fasciculus, OR, MdlF, clinical implication, functional outcome, parallel processing, and age-related change involved Boolean operators for the critical refining of the search in order to ensure all relevant literature was included.

Inclusion and exclusion criteria

The inclusion criteria in this umbrella review were chosen so that only the studies that provided relevant and high-quality insights regarding the position of the SS were included. Specifically, those using human subjects or human brain specimens were covered in order to have direct general applicability to all potential clinical practices. The studies included were human subject studies investigating the structure of the SS, its functional significance, and its clinical implications, with a focus on disruption to this structure and the ensuing effects on cognitive and sensory functions.

The preferential selection has focused on original research, case reports, retrospective studies, systematic reviews, as well as other relevant observational studies, through which many SSs and related WM tracts’ insights could be better uncovered. Specifically preferred are studies that provide data on the functional outcomes associated with SS damage in general and age-related changes, visual, language, and cognitive impairments. Exclusion criteria were applied for relevance and applicability to ensure only studies conducted on matter tracing the SS or its related deep WM tracts. Furthermore, included were studies that focused on this area rather than more general studies looking at it as an entity. Studies published in another language that did not offer an English version for translation were also ruled out to remove the possibility of flawed interpretation and to conduct an exhaustive review. Finally, studies performed exclusively in animals will be excluded, as there should be a clear relation in content to human anatomy or clinical practice, so it will be applicable for the important aim of offering knowledge that will be useful for understanding human neurological function and clinical outcomes.

Data extraction and analysis

The extraction of data was done very systematically, aiming at a full and accurate representation of the study findings from the selected studies. The extracted data included characteristics of the main studies, such as the author, year of publication, country, design, populations under study, and patient demographics, which formed a general background for each study. More so, comprehensive information was acquired regarding the point of focus anatomically, which, in this case, was centered on WM tracts within the SS and their interconnectivity in an attempt to understand the structural and functional role of these tracts.

Further, the functional roles of the SS and its related WM tracts were another critical section with regard to data extraction and allowed the identification of contributions that the SS made to various cognitive and sensory processes. These contributed to establishing relationships between anatomical structures and clinical outcomes.

Consequently, there were carefully documented, in many articles, a number of clinical implications of damage to the SS, particularly regarding visual, language, and cognitive functions, along with age-related changes that could exacerbate noted effects. Besides that, it was also documented which neuroimaging and intraoperative techniques the studies used in order to determine the methodologies that went into the investigation of the SS. This was an important piece of information since it would tell how the anatomical and functional data were obtained and the obtained findings’ reliability.

Two researchers independently reviewed the analysis for accuracy and appropriateness. Any disparity in the reflections regarding the reviews was discussed, and mutual consent led to the production of the final synthesis, which rests on the foundation of accurate and agreed-upon data. Qualitative synthesis was performed with an emphasis on the identification of common themes and patterns such that the results of all these studies could be comprehensively understood in terms of the role of the SS in neurological function and the clinical implications of damage to the SS.

Quality assessment

The tool Risk of bias in non-randomized studies(ROBINS-I) was used to determine that the studies included do not have a biased nature so that the findings can be generalized and have validity. The quality assessment is attached in Table 1 . Two independent assessors evaluated the quality of the included studies using the ROBINS-I tool. Any discrepancy in quality between the reviewers was resolved by discussion among themselves. These evaluations assigned every study to the low, moderate, severe, or critical categories of risk of bias. Only the studies judged to have a low or, at most, moderate risk of bias were carried forward for the final syntheses so that the conclusions were based on the most reliable evidence.

Table 1:

Risk of bias assessment using ROBINS-I tool of the included studies.

Synthesis of results

These findings were synthesized into common themes and patterns across the data in a qualitative manner. Studies were grouped with respect to functional outcomes, such as visual, language, and cognitive, and the effects of damage to SS, with special emphasis on age-related considerations. The synthesis would establish a deep understanding of the role SS plays in neurological functioning and the clinical implications of its damage in relation to neurosurgical interventions.

Ethical considerations

Since this was a review of available literature, no new data was to be collected from human subjects; therefore, no ethical approvals were needed. The included studies were checked for reporting that they had adhered to ethical standards.

RESULTS

Demographic and clinical characteristics

The studies included in this review span a diverse demographic range, encompassing patients of various ages, genders, and clinical conditions, all of which provide a broad basis for understanding the implications of SS damage [ Table 2 ].[ 1 - 4 , 6 , 7 , 9 - 17 , 20 , 22 , 23 , 25 - 27 , 30 , 31 ] The demographic data reveal that most patients involved in the studies were middle-aged adults, with mean ages ranging from 38 to 45 years across different studies. This age bracket was considered of particular interest because it covered that time window in life when the interplay between changes due to WM aging and those due to damage from disease is at its peak. Most of the patients in both populations were right-handed, with few being left-handed, and included both males and females; therefore, generalization of the findings would go for all subgroups.

Table 2:

Comprehensive data extraction and analysis of studies investigating SS damage: Anatomical, functional, and surgical outcomes.

These demographic findings are important, as they suggest that age, handedness, and baseline cognitive function could all be critical modifiers of the functional outcomes after SS damage and may affect the effectiveness of surgical interventions. Older patients, in particular, could be more sensitive to long-term risks for chronic cognitive decline due to added effects from the degeneration of WM with aging on top of disease-induced damage.

Anatomical organization and connectivity

The SS contains some WM tracts of key interest in cognitive and sensory processing. Among these, OR assumes a special position in relation to visual processing [ Figure 1 ]. They conduct visual information from the lateral geniculate nucleus to the visual cortex; the feature of laterality is notable here. In the left hemisphere, the OR processes information from the right visual field, and in the right hemisphere, that of the left. Lateralization, on the other hand, ensures that visual input from the contralateral visual field for both hemispheres is integrated in order to result in coherent visual perception.

Figure 1:

Illustrative representation of the SS and associated white matter tracts in the brain. (a) Lateral view of the brain surface for anatomical orientation. (b) Visualization of the sagittal stratum and its connections with the inferior longitudinal fasciculus and middle longitudinal fasciculus. The angular fasciculus and intraparietal sulcus are shown in relation to the SS.(c) Detailed view showing the SS in relation to the corona radiata, dorsal claustrum, and ILF. (d) The deep layer of the SS and its relationship to the dorsal claustrum, amygdaloid body, and hippocampal body. (e) Illustration of the optic radiation, including Meyer’s loop and its connectivity with the SS. AF/SLF: Arcuate fasciculus / Superior longitudinal fasciculus, Hipp. Body: Hippocampal body, IFOF stands for Inferior fronto-occipital fasciculus, ILF: Inferior longitudinal fasciculus, IPS: Intraparietal sulcus, LGB: Lateral geniculate body, MdLF: Middle longitudinal fasciculus, OT: Optic tract, OR: Optic radiation, SS: Sagittal stratum

Another critical tract in the SS is the inferior longitudinal fasciculus, which interconnects the occipital and temporal lobes. This kind of interconnection may be relevant to the procedures of visual identification and memory integration. Interestingly, the participation of the left ILF is overwhelmingly dominant in lexical access and linking faces to their names. In contrast, right ILF involvement can include nonverbal semantic processing and emotional recognition; it participates in face recognition and visual memory, predominantly across individuals with atypical linguistic lateralization, such as left-handers.[ 4 ]

The inferior frontal-occipital fasciculus forms the ventral pathway of visual stimulation and provides a critical route for the integration of visual stimuli with past experiences stored as conceptual knowledge. The IFOF subserves both verbal and nonverbal semantic processes, although it is dominant on the left side for language comprehension and visual-language integration. However, the right IFOF has a greater role in nonverbal tasks, interprets facial expressions, and recognizes objects.[ 2 ]

The other important constituents of the SS include the superior longitudinal fasciculus (SLF) and the arcuate fasciculus (AF). These tracts are fundamental ways of interconnecting language-related areas to support cognitive functions such as spatial working memory and social cognition. For example, the left SLF is heavily involved in language processing, specifically phonological and articulatory functions. In contrast, the right SLF is involved in social cognition and emotional regulation, with changes in this tract contributing to conditions such as social anxiety disorder.[ 2 , 29 ]

Functional implications of SS damage

Damage to the SS and its associated tracts can cause substantial functional impairments, although the specific outcomes often depend on the laterality of the affected tracts [ Table 3 ].[ 1 , 2 , 4 , 13 , 29 ] The OR are part of the SS and are significant in visual processing by transmitting information from the lateral geniculate nucleus to the visual cortex. The left OR mainly processes the right visual field, and the right OR processes the left visual field. This lateralization is what ensures each hemisphere integrates the contralateral input to light for coherent visual perception. These tracts can be damaged to cause visual field deficits, such as quadrantanopia or hemianopia, depending on the side of the lesion.[ 1 ]

Table 3:

Functional lateralization of the sagittal stratum components.

While the inferior longitudinal fasciculus (ILF) has been related to the integration of visual recognition and memory, different functions laterally remain relatively less known. The left ILF is more concerned with proper name retrieval, especially face-name association, and lexical access, interconnecting the occipital and temporal regions essential for visual recognition and word retrieval. The right ILF, on the other hand, is more involved in face recognition and visual working memory processing. It makes a large contribution to cross-hemispheric processing in individuals with both right- and left-handers or those who have atypical language lateralization. In addition, the right ILF may also subserve nonverbal semantic processing and emotion recognition via projections to the temporal lobe—and thus is crucially placed in integrating visual stimuli with emotional context.[ 4 ]

The IFOF is essential in linking visual stimuli to conceptual knowledge and has lateralized functions playing a crucial role in verbal and nonverbal semantic cognition. On the left, IFOF subserves language comprehension and visual-language integration via semantic processing, while on the right, it contributes significantly to nonverbal tasks—mostly in the realm of visual-semantic processing, such as facial expression interpretation and object recognition. Damage to the left IFOF has been associated with language deficits, and in particular with difficulties in linking visual input to semantic meaning. In contrast, damage to the right IFOF can affect the meaning given to visual stimuli and nonverbal cues, including facial expressions, underlining its role in nonverbal semantic cognition.[ 2 ]

The superior longitudinal fasciculus (SLF) and the AF play important roles in interconnecting language-related areas and supporting a number of other higher cognitive functions; their roles also significantly lateralize. The left SLF is especially concerned with language processing— particularly in connecting receptive and expressive language areas—and plays a crucial role in spatial working memory and coordinating complex cognitive functions related to language and attention. On the other hand, the right SLF is part of the interplay between occipito-temporal regions and prefrontal areas that take part in social cognition, emotional regulation, and face processing. The right SLF has lately been implicated in social anxiety disorder, thus showing its involvement in emotional and social processing.[ 2 , 29 ] Similarly, language processing primarily involves the left AF, including phonological processing, language comprehension, and verbal memory. Although some nonverbal cognitive functions are interested in the right AF, generally, it has worse performance in language tasks compared to the left AF. Therefore, damage to these tracts can cause language and social cognition deficits, whose specific impairments are based on the side of the damage.[ 18 ]

The thalamocortical radiations are critically involved in executive functions, including attention, cognitive efficiency, and problem-solving. It has been proven that there is a high correlation between the left thalamocortical pathway integrity and good cognitive outcomes. Thalamocortical radiations may also intervene healthily in mental flexibility, inhibition, and shifting. Along with the left thalamocortical pathway, an executive function is also supported by the right thalamocortical pathway, particularly the aspects of attention and cognitive efficiency. WM microstructure changes in the right thalamocortical fibers have been reported as related to executive dysfunction, mainly in children affected by epilepsy. This position emphasizes its integral role in the global process of sensorial integration and maintenance of “cognitive flexibility.”[ 19 ]

Surgical considerations and outcomes

The SS, with its associated WM tracts, is involved in maintaining a wide range of cognitive, sensory, and motor functions. Surgical interventions for SS, mainly gliomas and other brain lesions, need adequate preplanning and intraoperative strategies to reduce postoperative deficits. The current discourse synthesizes findings from multiple studies and then points out the surgical considerations and outcomes related to interventions close to the SS.

Intraoperative DES has already become a “gold standard” for awake brain surgery aimed at the resection of the tumors situated in close relations with the critical SS tracts with the goal of preserving relevant functions. The case description by Fernández Coello et al. (2013)[ 12 ] presents this approach implemented in a 41-year-old male patient with a low-grade glioma located in the right basal temporo-occipital region. Preoperative magnetic resonance imaging (MRI) and intraoperative DES enabled a careful mapping of the right ILF such that it was spared, and only a mild left superior quadrantanopia occurred, which resolved within 3 months and contributed to the severe deterioration of visual recognition functions. Rolland et al. (2018)[ 27 ] conducted a series of awake surgeries on 14 patients with right inferior parietal lobule gliomas. They revealed the complex SS connectivity, mainly the preservation of multiple tracts, including the superior longitudinal fasciculus and the inferior frontal-occipital fasciculus. Most patients recovered within 3 months, but four had persistent left superior quadrantanopia, which shows the importance of accurate functional mapping in order to avoid permanent sensory and cognitive deficits.

Laterality of the affected SS tracts has a significant bearing on the type of functional deficits observed postoperatively. ChanSeng et al. (2014)[ 6 ] studied the surgical outcomes of gliomas that involved the left SS of the brain with a concentration on problems that overcome the preservation of language and visual functions. Their results showed that intraoperative stimulation of IFOF could cause semantic paraphasia and that disruption of OR resulted in visual field deficits, mainly quadrantanopia. Despite these risks, the majority of these patients reverted to normal neurological function within 3 months, with few long-term impairments, thus suggesting that effective mapping and surgical techniques can mitigate the impact of left-sided resections. In contrast, Berro et al. (2021)[ 3 ] focused on right-sided resections, which are usually associated with nonverbal semantic cognition and visual-spatial processing. As previously described, in 17 patients with diffuse low-grade gliomas, although with nine developing left superior quadrantanopia, there was no long-term cognitive deficit. This indicates the divergence in functional risks associated with right- and left-sided surgeries and the need to preserve tracts such as the ILF and IFOF and also to preserve functions involving visual-space and nonverbal cognitive function.

Age is thus an essential consideration in surgical planning because age-related WM degeneration can exaggerate the effects of SS damage. Robles et al. (2022)[ 26 ] recorded the effects of traumatic brain injury (TBI) on WM tracts, including SS, across a rather wide span of ages. This study demonstrated significant reductions of fractional anisotropy (FA) values in major tracts such as ILF and corpus callosum, with a preferential focus on the same in cases where cerebral microbleeds were present in older patients. The findings thus suggest that, probably due to preexisting WM degradation, older patients are more at risk for cognitive decline after SS surgery and certainly warrant more cautious surgical strategies among this age group. Latini et al. (2017)[ 17 ] took it further by making efforts to explain the challenges of doing procedures on the elderly through a study on the segmentation and connectivity of the ILF. Their worry revealed that the age erosion of the ILF led it to have detection on the visual and memory functions, which the surgery further affected. This tract is particularly important in older patients for the prevention of accelerated cognitive decline and quality of life preservation.

Long-term recovery and rehabilitation

Overall, long-term functional recovery after SS surgery is quite good if the critical tracts are preserved. Duffau et al. (2005, 2008)[ 9 , 10 ] did detailed studies on language function recoveries after glioma resection in the dominant hemisphere. Their studies showed that patients, even if they developed language deficits such as aphasia or semantic paraphasia in the immediate postoperative period, recovered to their baseline or better in 3–6 months. Recovery is supported by plasticity and intraoperative subcortical mapping of the brain, whereby tumors can be safely resected. In contrast, the essential language pathways in the brain are preserved, and the methodology is okay with regard to the preservation of structures like the AF and IFOF. Wu et al. (2016)[ 31 ] extended this research to various subcomponents of the IFOF using DSI and tractography. This study showed that the IFOF is a multi-component tract involved in both visual-spatial and language functions. The authors, therefore, emphasize the need for detailed preoperative imaging and intraoperative mapping to identify and preserve these subcomponents during surgery to achieve optimal long-term recovery with the smallest possible degree of functional deficit.

Neuroimaging and surgical planning

Advanced neuroimaging modalities form an intrinsic part of surgical planning and execution of procedures at the SS. Hosoya et al. (1998)[ 16 ] assessed, in a cross-sectional study by MRI, the anatomy of WM layers surrounding the trigone of the lateral ventricle, including the SS. Their findings showcase the importance of careful MRI analysis in the identification of distinct WM layers participating during both visual and sensory processing. It is a complex organization of the tapetum and internal SS; understanding the details of these layers is important for neurosurgeons seeking to retain as much sensory function as possible during surgery, particularly in older patients where WM integrity is already compromised. Eichert et al. (2019)[ 11 ] provided further insight into the neuroanatomical underpinnings of the SS through a comparative study involving humans and macaques with diffusion-weighted MRI and probabilistic tractography. It showed rectilinear, grid-like WM tract organization, including that of the SS and SLF, which underpins the functional integrity and adaptability of the brain with significant implications for the preservation of cognitive function within surgical intervention. Such disruptions to this grid structure may have important implications, particularly in patients undergoing resection of tumors near these critical pathways.

Preservation of the critical SS pathways during surgery is very important for minimizing functional deficits and ensuring a high quality of life after surgery. According to the accumulated literature, advanced neuroimaging techniques support methods of intraoperative mapping and require sophisticated knowledge of the complex connectivity within the SS to guide surgical decisions. Neurosurgeons should make continuous, unremitting attempts to use the latest techniques and strategies to tide over such challenges, as our understanding of the SS and the associated tracts is ever evolving.

Although SS surgeries carry critical cognitive and sensory risks, the evidence shows that they can be avoided with careful surgical planning, consideration of the patient’s condition, and utilization of advanced intraoperative methods. Future research should further elucidate the long-term outcomes of SS surgeries, particularly age-related differences and possible neural recovery in various populations.

Age-related implications of SS damage

There are important age-related implications for the damage to the SS, especially because aging alone tends to result in the natural degeneration of WM tracts. This degeneration might contribute to the impact of damage in the SS on cognitive and sensory outcomes and may mitigate any outcome advantage observed in older compared with younger subjects.

Little wonder that, in aging, WM structural integrity is generally lowered for key tracts within the SS: ILF and IFOF. It has been demonstrated that this age-related degradation is most rigid in ILF and IFOF—the core pathways related to visual recognition, memory integration, and semantic processing. The natural decline in these tracts’ integrity contributes to an increased vulnerability to cognitive impairments, such as memory deficits and difficulties in visual processing, particularly in tasks that require the integration of visual stimuli with semantic knowledge. For instance, Robles et al. (2022)[ 26 ] reported that older adults with TBI had dramatic WM loss in the corpus callosum and superficial frontal and temporal fasciculi, locations belonging to or connecting to the SS. Their findings concluded that age is an important predictor of post-TBI cognitive decline in people alongside the presence of cerebral microbleeds. This probably puts older adults at a greater risk of suffering more severe cognitive impairments following SS damage, likely because of the combined effects of aging and reduced plasticity of the aging brain.

Moreover, diminished neural plasticity in elderly patients reduces the chances of recovery from SS damage. The fact that young individuals have a less plastic brain compared to older ones also implies that some compensation/reorganization after injury does occur in the higher-plasticity brain. In contrast, similar damage in the elderly is more likely to result in permanent deficits because of the lesser plasticity of the brain. This impact is best viewed concerning surgical interventions associated with the SS because patients are more likely to have long-term cognitive and sensory deficits if critical WM tracts are damaged during surgical procedures.

Additionally, age-related changes have an impact on neurosurgical outcomes through changes to WM. For instance, studies like those by Chan-Seng et al. (2014)[ 6 ] and Berro et al. (2021)[ 3 ] provide evidence that the surgical planning and mapping during the surgeons’ glioma resection in elderly patients were actually suggested for the preservation of key SS tracts. In this regard, the compounding effects of natural WM degeneration and surgical trauma worsen cognitive and visual impairments; thus, damage should be minimized during surgery to these tracts.

In summary, aging processes are a prominent modifier of SS damage outcome, with older individuals more likely to present with cognitive and sensory impairments from both naturally occurring degeneration and decreased neural plasticity. This underlies the importance of age-related considerations in the diagnosis, treatment, and surgical management of pathologies concerning SS.

Synthesis of key findings

This review has indicated disruption to the SS and its cluster WM tracts in a variety of higher-order cognitive and sensory functions. Anatomically, the SS itself proved to be a complex and multilayered structure. Highly lateralized, these tracts have specific functional roles dependent upon their hemispheric location. Functionally, these could result in huge SS damages to the process of vision, comprehension of language, and even cognitive functions, with the degree and nature frequently modulated by the affected tract and its lateralization. These findings have important ramifications for surgical interventions, in which awake brain mapping is used to aid in preserving critical functions and minimizing long-term deficits, especially in older subjects.

In conclusion, this review provides an in-depth understanding of the anatomical and functional importance of the SS and, therefore, the need for careful surgical planning with consideration of age-related changes to optimize the benefit for patients.

DISCUSSION

Within neurosurgical interventions, the SS holds a special place because approximately 60% of all brain tumors, including gliomas, reside in eloquent regions where the integrity of the surrounding WM tracts needs to be maximally preserved to prevent significant postoperative deficits.[ 24 ] The SS connects the brain to various WM tracts important for the integration of sensory inputs that underpin higher-order cognitive processes. The complexity of connectivity within the SS itself, including tracts such as the IFOF, OR, and SLF, underlies this structure’s critical role in maintaining normal brain function. Damage to the SS resulting from disease or surgical intervention can result in profound deficits, particularly against a backdrop of age-related changes. This discussion synthesizes findings from an extensive body of literature reviewed for SS damage functional outcomes as related to aspects of laterality, challenges of aging, and the critical inclusion of advanced surgical techniques.

Functional results of SS damage are importantly lateralized so that specific patterns of impairment have been associated with the damage of the left or right hemisphere. In reviewing the studies, this paper has shown that SS damage on the left side is often associated with major deficits in language and visual processing. For example, Chan-Seng et al. (2014)[ 6 ] reported that lesions in the left IFOF give rise to semantic paraphasia, generating a severe disruption of language processing and production. This can create particular problems for patients scheduled for resections of gliomas in the dominant left hemisphere, where even slight perturbations of the IFOF may promote chronic linguistic deficits. Similarly, lesions of the left OR entail visual field deficits, such as quadrantanopia, which compromises the processing of visual information emanating from the contralateral visual field. This lateralized processing of visual information underlies coherent visual perception, and damage to the OR could have important consequences for the ability of a patient to move about freely and interact with their environment.[ 1 ]

In contrast, right-sided damage will more likely involve nonverbal cognition and aspects of visual-spatial processing. Berro et al. (2021)[ 3 ] showed that right-sided resections at this level of the ILF usually result in deficits in visual recognition memory, especially for tasks integrating visual stimuli with emotional or spatial context. This puts a premium on the preservation of the right ILF during surgery for the preservation of these higher-order cognitive functions. The right SLF connects occipitotemporal regions with prefrontal areas and is crucial for social cognition and emotional regulation; damage to this tract has been implicated in disorders as diverse as social anxiety disorder, therefore also underscoring the essence of these meticulous surgical plannings when operating in these areas.

Another critical component of the SS includes the thalamocortical radiations interconnecting the thalamus with the cerebral cortex. These tracts play a critically important role in executive functions for attention, cognitive efficiency, and problem-solving. Law et al. (2018)[ 18 ] emphasized the preservation of such connections, particularly in pediatric temporal lobe epilepsy patients, where interruptions to the thalamocortical pathways may result in important cognitive deficits. Their findings underline the need for highly accurate surgical techniques that will cause minimal damage to these tracts, especially in younger patients in whom the possibility for long-term cognitive impact is very high.

One of the major confounding variables within SS damage management is aging, whose degenerating process with age significantly worsens surgical- and disease-related disruptions in WM tracts. Robles et al. (2022)[ 26 ] provided very compelling evidence that older individuals are more at risk of late-onset cognitive decline after SS surgery, more so in the presence of pre-existing conditions like cerebral microbleeds. Their findings included a significant decline in FA in important tracts, like the ILF and the corpus callosum, indicating patients are at an increased risk for postoperative cognitive impairment. This places a sharp focus on the imperative need for surgical age-specific strategies that account for reduced plasticity and enhanced vulnerability of the maturing brain. Latini et al. (2017)[ 17 ] extended the investigation into how SS damage affects older patients with a study on the segmentation of the ILF and its connectivity in aging. Their results evidenced that age-related degradation may well contribute to dramatic failures of visual and memory functions worsened by surgical interventions in the ILF. This tract is of essence to be preserved in older adults to prevent an accelerated cognitive decline and impairment of quality of life. The results further support the surgical strategies that are compared to the possible vulnerabilities of the old aging brain.

Besides these structural concerns, neural plasticity is reduced in older adults, which complicates the recovery from damage to the SS. Because neural plasticity is higher in the young, the damage can often be compensated for by changing the organization of brain networks. A similar amount of damage may result in more permanent deficits in older adults because their aging brain lacks such adaptability. This is especially evident in visual and memory functions, where any recovery is limited by age-related degradation of WM. Additive effects of aging and SS damage call for older patients to follow a more cautious surgical approach.

Recent research into the cerebral WM myelination process has greatly improved knowledge of how age, gender, and cognitive functions are intertwined in brain development at crucial white-matter pathways, such as the SS. Myelination is one critical process that enables efficient neural transmission that significantly changes across the lifespan and thus impacts cognitive ability and the overall functional integrity of the brain. As Buyanova and Arsalidou (2021)[ 5 ] convincingly argue in their competitive review, the decline in myelination with age, especially of the IFOF and SLF, reduces the threshold for older adults to acknowledge cognitive impairments due to SS injuries. Most recently, it also brought attention to sex/gender variations in WM development, which may further modulate cognitive outcomes subsequent to SS injury. In particular, this differential rate and extent of myelination may introduce variations within male and female brains in terms of response to damage, thereby indicating possible gender-specific therapeutic strategies on the one hand for clinical diagnosis and surgical interventions on the other. Putting all these findings together into the general context of SS research points out that individual variability in myelination is a factor that should be controlled when trying to quantify the overall impact of SS damage. Such an approach could provide more individualized strategies for the management and mitigation of SS injury effects, particularly in aging populations in whom WM integrity is already somewhat compromised.

Preservation of SS tracts at surgery is important to reduce postoperative deficits and to have good long-term outcomes. Progress in neuroimaging and intraoperative mapping has dramatically enhanced a neurosurgeon’s possibility to recognize and spare critical pathways during brain surgery. Wu et al. (2016)[ 31 ] reported that diffusion tensor imaging (DTI) and tractography displayed SS tracts, for example, the IFOF, in detail, thus providing surgeons with information to avoid these critical areas in its resection. The utility of the technique has been greatest in surgeries for gliomas, where the potential for mapping and preserving language and visual pathways may make a great deal of difference in postoperative quality of life. Awake brain surgery has become a gold standard in preserving function during SS surgeries due to DES on its own during procedures. This approach was demonstrated to be effective in keeping one’s abilities in visual recognition and spatial processing by Fernández Coello et al. (2013)[ 12 ] and, more recently, by Rolland et al. (2018).[ 27 ] These findings underline the importance of real-time functional mapping in preserving the critical SS pathways and reducing the risk of permanent deficits. Extensive research on language function recovery after glioma resection in the dominant hemisphere by Duffau et al. (2005, 2008)[ 9 , 10 ] showed that even in patients with an initial deficit, such as aphasia or semantic paraphasia, most recovered to baseline or better within 3–6 months. It is promoted by the plasticity of the brain and intraoperative subcortical mapping, which enables safe tumor resection that does the least damage to essential language pathways, including the AF and IFOF. These results underline the fact that surgical preservation of the critical tracts is basic in sustaining long-lasting functional recovery.

The findings of the current study provide further support for the need for more research into the functional implications of SS damage and the refining of surgical techniques. With the evolving knowledge of the SS and its associated tracts, the need for further research persists into the long-term outcomes of SS surgeries, particularly in different age groups. Future studies should be more focused on the potential for neural recovery in older people and on developing interventions that can enhance this recovery, possibly mitigating the effects of WM degradation with age. On a clinical level, these results point out the need for surgical planning. Some forms of advanced neuroimaging and intraoperative mapping should be standard in SS surgeries to preserve the most critical pathways and thereby avoid deficits in the patient following the surgery.

In that sense, it is of great necessity that during surgery, the SS and all of its tracts be preserved to minimize possible functional impairments, ensuring a high quality of life for the patients. The results support further findings and clinical applications that underscore the necessity of a nuanced approach to SS in neurological function, with a proportional value of surgical methods for tailoring approaches according to the challenges that WM changes appear to pose throughout the aging process.

CONCLUSION

In conclusion, the SS plays a crucial role in integrating sensory, cognitive, and motor functions, making its preservation essential during neurosurgical procedures, particularly in older adults who may already have compromised WM integrity. Advances in neuroimaging and intraoperative techniques, such as DTI and DES, have significantly reduced the risks associated with SS damage. Ongoing research and the refinement of surgical approaches are vital to minimize the impact of SS injury further, ultimately aiming to improve patient outcomes and quality of life following surgery.

Ethical approval

Institutional Review Board approval is not required.

Declaration of patient consent

Patient’s consent not required as there are no patients in this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

Acknowledgment

We would like to express our gratitude to Mohammed A. Bani Saad for providing the illustrative image and for his exceptional effort in creating and drawing it.

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