Anterior Ectosylvian Sulcus Research Articles

Association Cortex Is Essential to Reverse Hemianopia by Multisensory Training.

Hemianopia induced by unilateral visual cortex lesions can be resolved by repeatedly exposing the blinded hemifield to auditory-visual stimuli. This rehabilitative "training" paradigm depends on mechanisms of multisensory plasticity that restore the lost visual responsiveness of multisensory neurons in the ipsilesional superior colliculus (SC) so that they can once again support vision in the blinded hemifield. These changes are thought to operate via the convergent visual and auditory signals relayed to the SC from association cortex (the anterior ectosylvian sulcus [AES], in cat). The present study tested this assumption by cryogenically deactivating ipsilesional AES in hemianopic, anesthetized cats during weekly multisensory training sessions. No signs of visual recovery were evident in this condition, even after providing animals with up to twice the number of training sessions required for effective rehabilitation. Subsequent training under the same conditions, but with AES active, reversed the hemianopia within the normal timeframe. These results indicate that the corticotectal circuit that is normally engaged in SC multisensory plasticity has to be operational for the brain to use visual-auditory experience to resolve hemianopia.

Differential distributions of parvalbumin-positive interneurons in the sulci and gyri of the adult ferret cerebral cortex

Although accumulating evidence suggests that there are significant anatomical and histological differences between the sulci and gyri of the cerebral cortex, whether there is a difference in the distribution of interneurons between the two cortical regions remains largely unknown. In this study, we systematically compared the distributions of parvalbumin-positive interneurons among three neighboring gyrus and sulcus pairs-coronal gyrus and cruciate sulcus, anterior ectosylvian gyrus and rostral suprasylvian sulcus, and posterior ectosylvian gyrus and pseudosylvian sulcus-in the adult ferret cerebral cortex. We proposed a method to partition sulci and gyri into several specific subregions through the deepest points of the sulci and the highest points of gyri in the inner and outer cortical contours of coronal sections. We found that the density of parvalbumin-positive interneurons in the gyri was significantly higher than that in the sulci. Further study revealed that the density of PV interneurons in superficial cortical layers (layers 2/3 and layer 4) was comparable among the three pairs of sulci and gyri. However, the density of parvalbumin-positive interneurons in cortical layers 5/6 was significantly higher in gyri than in sulci. These results indicate that parvalbumin-positive interneurons are differently distributed in infragranular layers of cortical sulci and gyri.

A multimodal pathway including the basal ganglia in the feline brain.

The purpose of this paper is to give an overview of our present knowledge about the feline tecto-thalamo-basal ganglia cortical sensory pathway. We reviewed morphological and electrophysiological studies of the cortical areas, located in ventral bank of the anterior ectosylvian sulcus as well as the region of the insular cortex, the suprageniculate nucleus of the thalamus, caudate nucleus, and the substantia nigra. Microelectrode studies revealed common receptive field properties in all these structures. The receptive fields were extremely large and multisensory, with pronounced sensitivity to motion of visual stimuli. They often demonstrated directional and velocity selectivity. Preference for small visual stimuli was also a frequent finding. However, orientation sensitivity was absent. It became obvious that the structures of the investigated sensory loop exhibit a unique kind of information processing, not found anywhere else in the feline visual system.

What and How the Deaf Brain Sees.

Over the past decade, there has been an unprecedented level of interest and progress into understanding visual processing in the brain of the deaf. Specifically, when the brain is deprived of input from one sensory modality (such as hearing), it often compensates with supranormal performance in one or more of the intact sensory systems (such as vision). Recent psychophysical, functional imaging, and reversible deactivation studies have converged to define the specific visual abilities that are enhanced in the deaf, as well as the cortical loci that undergo crossmodal plasticity in the deaf and are responsible for mediating these superior visual functions. Examination of these investigations reveals that central visual functions, such as object and facial discrimination, and peripheral visual functions, such as motion detection, visual localization, visuomotor synchronization, and Vernier acuity (measured in the periphery), are specifically enhanced in the deaf, compared with hearing participants. Furthermore, the cortical loci identified to mediate these functions reside in deaf auditory cortex: BA 41, BA 42, and BA 22, in addition to the rostral area, planum temporale, Te3, and temporal voice area in humans; primary auditory cortex, anterior auditory field, dorsal zone of auditory cortex, auditory field of the anterior ectosylvian sulcus, and posterior auditory field in cats; and primary auditory cortex and anterior auditory field in both ferrets and mice. Overall, the findings from these studies show that crossmodal reorganization in auditory cortex of the deaf is responsible for the superior visual abilities of the deaf.

Distribution and Morphology of Cortical Terminals in the Cat Thalamus from the Anterior Ectosylvian Sulcus

Two main types of cortical terminals have been identified in the cat thalamus. Large (type II) have been proposed to drive the response properties of thalamic cells while smaller (type I) are believed to modulate those properties. Among the cat’s visual cortical areas, the anterior ectosylvian visual area (AEV) is considered as one of the highest areas in the hierarchical organization of the visual system. Whereas the connections from the AEV to the thalamus have been recognized, their nature (type I or II) is presently not known. In this study, we assessed and compared the relative contribution of type I and type II inputs to thalamic nuclei originating from the AEV. The anterograde tracer BDA was injected in the AEV of five animals. Results show that (1) both type I and II terminals from AEV are present in the Lateral Posterior- Pulvinar complex, the lateral median suprageniculate complex and the medial and dorsal geniculate nuclei (2) type I terminals significantly outnumber the type II terminals in almost all nuclei studied. Our results indicate that neurons in the AEV are more likely to modulate response properties in the thalamus rather than to determine basic organization of receptive fields of thalamic cells.

Do the Different Sensory Areas Within the Cat Anterior Ectosylvian Sulcal Cortex Collectively Represent a Network Multisensory Hub?

Current theory supports that the numerous functional areas of the cerebral cortex are organized and function as a network. Using connectional databases and computational approaches, the cerebral network has been demonstrated to exhibit a hierarchical structure composed of areas, clusters and, ultimately, hubs. Hubs are highly connected, higher-order regions that also facilitate communication between different sensory modalities. One region computationally identified network hub is the visual area of the Anterior Ectosylvian Sulcal cortex (AESc) of the cat. The Anterior Ectosylvian Visual area (AEV) is but one component of the AESc that also includes the auditory (Field of the Anterior Ectosylvian Sulcus - FAES) and somatosensory (Fourth somatosensory representation - SIV). To better understand the nature of cortical network hubs, the present report reviews the biological features of the AESc. Within the AESc, each area has extensive external cortical connections as well as among one another. Each of these core representations is separated by a transition zone characterized by bimodal neurons that share sensory properties of both adjoining core areas. Finally, core and transition zones are underlain by a continuous sheet of layer 5 neurons that project to common output structures. Altogether, these shared properties suggest that the collective AESc region represents a multiple sensory/multisensory cortical network hub. Ultimately, such an interconnected, composite structure adds complexity and biological detail to the understanding of cortical network hubs and their function in cortical processing.

Is territorial expansion a mechanism for crossmodal plasticity?

Crossmodal plasticity is the phenomenon whereby, following sensory damage or deprivation, the lost sensory function of a brain region is replaced by one of the remaining senses. One of several proposed mechanisms for this phenomenon involves the expansion of a more active brain region at the expense of another whose sensory inputs have been damaged or lost. This territorial expansion hypothesis was examined in the present study. The cat ectosylvian visual area (AEV) borders the auditory field of the anterior ectosylvian sulcus (FAES), which becomes visually reorganized in the early deaf. If this crossmodal effect in the FAES is due to the expansion of the adjoining AEV into the territory of the FAES after hearing loss, then the reorganized FAES should exhibit connectional features characteristic of the AEV. However, tracer injections revealed significantly different patterns of cortical connectivity between the AEV and the early deaf FAES, and substantial cytoarchitectonic and behavioral distinctions occur as well. Therefore, the crossmodal reorganization of the FAES cannot be mechanistically attributed to the expansion of the adjoining cortical territory of the AEV and an overwhelming number of recent studies now support unmasking of existing connections as the operative mechanism underlying crossmodal plasticity.

A quantitative comparison of the hemispheric, areal, and laminar origins of sensory and motor cortical projections to the superior colliculus of the cat.

The superior colliculus (SC) is a midbrain structure central to orienting behaviors. The organization of descending projections from sensory cortices to the SC has garnered much attention; however, rarely have projections from multiple modalities been quantified and contrasted, allowing for meaningful conclusions within a single species. Here, we examine corticotectal projections from visual, auditory, somatosensory, motor, and limbic cortices via retrograde pathway tracers injected throughout the superficial and deep layers of the cat SC. As anticipated, the majority of cortical inputs to the SC originate in the visual cortex. In fact, each field implicated in visual orienting behavior makes a substantial projection. Conversely, only one area of the auditory orienting system, the auditory field of the anterior ectosylvian sulcus (fAES), and no area involved in somatosensory orienting, shows significant corticotectal inputs. Although small relative to visual inputs, the projection from the fAES is of particular interest, as it represents the only bilateral cortical input to the SC. This detailed, quantitative study allows for comparison across modalities in an animal that serves as a useful model for both auditory and visual perception. Moreover, the differences in patterns of corticotectal projections between modalities inform the ways in which orienting systems are modulated by cortical feedback. J. Comp. Neurol. 524:2623-2642, 2016. © 2016 Wiley Periodicals, Inc.

Cortical and thalamic connectivity of the auditory anterior ectosylvian cortex of early-deaf cats: Implications for neural mechanisms of crossmodal plasticity

Early hearing loss leads to crossmodal plasticity in regions of the cerebrum that are dominated by acoustical processing in hearing subjects. Until recently, little has been known of the connectional basis of this phenomenon. One region whose crossmodal properties are well-established is the auditory field of the anterior ectosylvian sulcus (FAES) in the cat, where neurons are normally responsive to acoustic stimulation and its deactivation leads to the behavioral loss of accurate orienting toward auditory stimuli. However, in early-deaf cats, visual responsiveness predominates in the FAES and its deactivation blocks accurate orienting behavior toward visual stimuli. For such crossmodal reorganization to occur, it has been presumed that novel inputs or increased projections from non-auditory cortical areas must be generated, or that existing non-auditory connections were ‘unmasked.’ These possibilities were tested using tracer injections into the FAES of adult cats deafened early in life (and hearing controls), followed by light microscopy to localize retrogradely labeled neurons. Surprisingly, the distribution of cortical and thalamic afferents to the FAES was very similar among early-deaf and hearing animals. No new visual projection sources were identified and visual cortical connections to the FAES were comparable in projection proportions. These results support an alternate theory for the connectional basis for cross-modal plasticity that involves enhanced local branching of existing projection terminals that originate in non-auditory as well as auditory cortices.

Synaptic Basis for Cross-modal Plasticity: Enhanced Supragranular Dendritic Spine Density in Anterior Ectosylvian Auditory Cortex of the Early Deaf Cat.

In the cat, the auditory field of the anterior ectosylvian sulcus (FAES) is sensitive to auditory cues and its deactivation leads to orienting deficits toward acoustic, but not visual, stimuli. However, in early deaf cats, FAES activity shifts to the visual modality and its deactivation blocks orienting toward visual stimuli. Thus, as in other auditory cortices, hearing loss leads to cross-modal plasticity in the FAES. However, the synaptic basis for cross-modal plasticity is unknown. Therefore, the present study examined the effect of early deafness on the density, distribution, and size of dendritic spines in the FAES. Young cats were ototoxically deafened and raised until adulthood when they (and hearing controls) were euthanized, the cortex stained using Golgi-Cox, and FAES neurons examined using light microscopy. FAES dendritic spine density averaged 0.85 spines/μm in hearing animals, but was significantly higher (0.95 spines/μm) in the early deaf. Size distributions and increased spine density were evident specifically on apical dendrites of supragranular neurons. In separate tracer experiments, cross-modal cortical projections were shown to terminate predominantly within the supragranular layers of the FAES. This distributional correspondence between projection terminals and dendritic spine changes indicates that cross-modal plasticity is synaptically based within the supragranular layers of the early deaf FAES.

Cerebral origins of the auditory projection to the superior colliculus of the cat

The superior colliculus (SC) is critical for directing accurate head and eye movements to visual and acoustic targets. In visual cortex, areas involved in orienting of the head and eyes to a visual stimulus have direct projections to the SC. In auditory cortex of the cat, four areas have been identified to be critical for the accurate orienting of the head and body to an acoustic stimulus. These areas include primary auditory cortex (A1), the posterior auditory field (PAF), the dorsal zone of auditory cortex (DZ), and the auditory field of the anterior ectosylvian sulcus (fAES). Therefore, we hypothesized that these four regions of auditory cortex would have direct projections to the SC. To test this hypothesis, deposits of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were made into the superficial and deep layers of the SC to label, by means of retrograde transport, the auditory cortical origins of the corticotectal pathway. Bilateral examination of auditory cortex revealed that the vast majority of the labeled cells were located in the hemisphere ipsilateral to the SC injection. In ipsilateral auditory cortex, nearly all the labeled neurons were found in the infragranular layers, predominately in layer V. The largest population of labeled cells was located in the fAES. Few labeled neurons were identified in A1, PAF, or DZ. Thus, in contrast to the visual system, only one of the auditory cortical areas involved in orienting to an acoustic stimulus has a strong direct projection to the SC. Sound localization signals processed in primary (A1) and other non-primary (PAF and DZ) auditory cortices may be transmitted to the SC via a multi-synaptic corticotectal network.

Organization and Reorganization of Sensory-Deprived Cortex

The scientific literature has grown rich in research illustrating the remarkable ability of the brain to reorganize itself following sensory loss. In particular, visually deafferented regions within the occipital cortex of early blind individuals have been repeatedly shown to be functionally recruited to carry out a wide variety of nonvisual tasks. While the novelty of such a finding might be wearing off, more recent research has begun to examine whether this crossmodal takeover of the occipital cortex in blindness follows some sort of organizational principle. Here we first review the most recent evidence from neuroimaging studies that illustrate how the pre-existing functional specialization of cortical sub-regions appears to be preserved following sensory deprivation. We discuss and compare work on visual and auditory deprivation, as well as research on individuals with intact sensory systems. We suggest avenues for future exploration of these issues, such as identifying the neuroanatomical markers of crossmodal plasticity and elucidating the behavioral relevance of observed changes.

Direct projection from the visual associative cortex to the caudate nucleus in the feline brain

Recent morphological and physiological studies support the assumption that the extrageniculate ascending tectofugal pathways send visual projection to the caudate nucleus (CN) in amniotes. In the present study we investigate the anatomical connection between the visual associative cortex along the anterior ectosylvian sulcus (AES) and the CN in adult domestic cats. An anterograde tracer – fluoro-dextrane-amine – was injected into the AES cortex. The distribution of labeled axons was not uniform in the CN. The majority of labeled axons and terminal like puncta was found only in a limited area in the dorsal part of the CN between the coordinates anterior 12–15. Furthermore, a retrograde tracer – choleratoxin-B – was injected into the dorsal part of the CN between anterior 12 and 13. We detected a large number of labeled neurons in the fundus and the dorsal part of the AES between the coordinates anterior 12–14. Based upon our recent results we argue that there is a direct monosynaptic connection between the visual associative cortex along the AES and the CN. Beside the posterior thalamus, the AES cortex should also participate in the transmission of the tectal visual information to the CN. This pathway is likely to convey complex information containing both sensory and motor components toward the basal ganglia, which supports their integrative function in visuomotor actions such as motion and novelty detection and saccade generation.

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex.

It is well known that early disruption of sensory input from one modality can induce crossmodal reorganization of a deprived cortical area, resulting in compensatory abilities in the remaining senses. Compensatory effects, however, occur in selected cortical regions and it is not known whether such compensatory phenomena have any relation to the original function of the reorganized area. In the cortex of hearing cats, the auditory field of the anterior ectosylvian sulcus (FAES) is largely responsive to acoustic stimulation and its unilateral deactivation results in profound contralateral acoustic orienting deficits. Given these functional and behavioral roles, the FAES was studied in early-deafened cats to examine its crossmodal sensory properties as well as to assess the behavioral role of that reorganization. Recordings in the FAES of early-deafened adults revealed robust responses to visual stimulation as well as receptive fields that collectively represented the contralateral visual field. A second group of early-deafened cats was trained to localize visual targets in a perimetry array. In these animals, cooling loops were surgically placed on the FAES to reversibly deactivate the region, which resulted in substantial contralateral visual orienting deficits. These results demonstrate that crossmodal plasticity can substitute one sensory modality for another while maintaining the functional repertoire of the reorganized region.

Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32

The monoclonal antibody SMI-32 was used to characterize and distinguish individual areas of cat auditory cortex. SMI-32 labels non-phosphorylated epitopes on the high- and medium-molecular weight subunits of neurofilament proteins in cortical pyramidal cells and dendritic trees with the most robust immunoreactivity in layers III and V. Auditory areas with unique patterns of immunoreactivity included: primary auditory cortex (AI), second auditory cortex (AII), dorsal zone (DZ), posterior auditory field (PAF), ventral posterior auditory field (VPAF), ventral auditory field (VAF), temporal cortex (T), insular cortex (IN), anterior auditory field (AAF), and the auditory field of the anterior ectosylvian sulcus (fAES). Unique patterns of labeling intensity, soma shape, soma size, layers of immunoreactivity, laminar distribution of dendritic arbors, and labeled cell density were identified. Features that were consistent in all areas included: layers I and IV neurons are immunonegative; nearly all immunoreactive cells are pyramidal; and immunoreactive neurons are always present in layer V. To quantify the results, the numbers of labeled cells and dendrites, as well as cell diameter, were collected and used as tools for identifying and differentiating areas. Quantification of the labeling patterns also established profiles for ten auditory areas/layers and their degree of immunoreactivity. Areal borders delineated by SMI-32 were highly correlated with tonotopically-defined areal boundaries. Overall, SMI-32 immunoreactivity can delineate ten areas of cat auditory cortex and demarcate topographic borders. The ability to distinguish auditory areas with SMI-32 is valuable for the identification of auditory cerebral areas in electrophysiological, anatomical, and/or behavioral investigations.

Spatial receptive field organization of multisensory neurons and its impact on multisensory interactions

Previous work has established that the spatial receptive fields (SRFs) of multisensory neurons in the cerebral cortex are strikingly heterogeneous, and that SRF architecture plays an important deterministic role in sensory responsiveness and multisensory integrative capacities. The initial part of this contribution serves to review these findings detailing the key features of SRF organization in cortical multisensory populations by highlighting work from the cat anterior ectosylvian sulcus (AES). In addition, we have recently conducted parallel studies designed to examine SRF architecture in the classic model for multisensory studies, the cat superior colliculus (SC), and we present some of the preliminary observations from the SC here. An examination of individual SC neurons revealed marked similarities between their unisensory (i.e., visual and auditory) SRFs, as well as between these unisensory SRFs and the multisensory SRF. Despite these similarities within individual neurons, different SC neurons had SRFs that ranged from a single area of greatest activation (hot spot) to multiple and spatially discrete hot spots. Similar to cortical multisensory neurons, the interactive profile of SC neurons was correlated strongly to SRF architecture, closely following the principle of inverse effectiveness. Thus, large and often superadditive multisensory response enhancements were typically seen at SRF locations where visual and auditory stimuli were weakly effective. Conversely, subadditive interactions were seen at SRF locations where stimuli were highly effective. Despite the unique functions characteristic of cortical and subcortical multisensory circuits, our results suggest a strong mechanistic interrelationship between SRF microarchitecture and integrative capacity.

Multisensory Integration in the Superior Colliculus Requires Synergy among Corticocollicular Inputs

Influences from the visual (AEV), auditory (FAES), and somatosensory (SIV) divisions of the cat anterior ectosylvian sulcus (AES) play a critical role in rendering superior colliculus (SC) neurons capable of multisensory integration. However, it is not known whether this is accomplished via their independent sensory-specific action or via some cross-modal cooperative action that emerges as a consequence of their convergence on SC neurons. Using visual-auditory SC neurons as a model, we examined how selective and combined deactivation of FAES and AEV affected SC multisensory (visual-auditory) and unisensory (visual-visual) integration capabilities. As noted earlier, multisensory integration yielded SC responses that were significantly greater than those evoked by the most effective individual component stimulus. This multisensory "response enhancement" was more evident when the component stimuli were weakly effective. Conversely, unisensory integration was dominated by the lack of response enhancement. During cryogenic deactivation of FAES and/or AEV, the unisensory responses of SC neurons were only modestly affected; however, their multisensory response enhancement showed a significant downward shift and was eliminated. The shift was similar in magnitude for deactivation of either AES subregion and, in general, only marginally greater when both were deactivated simultaneously. These data reveal that SC multisensory integration is dependent on the cooperative action of distinct subsets of unisensory corticofugal afferents, afferents whose sensory combination matches the multisensory profile of their midbrain target neurons, and whose functional synergy is specific to rendering SC neurons capable of synthesizing information from those particular senses.

Axon Morphologies and Convergence Patterns of Projections from Different Sensory-Specific Cortices of the Anterior Ectosylvian Sulcus onto Multisensory Neurons in the Cat Superior Colliculus

Corticofugal projections to the thalamus reveal 2 axonal morphologies, each associated with specific physiological attributes. These determine the functional characteristics of thalamic neurons. It is not clear, however, whether such features characterize the corticofugal projections that mediate multisensory integration in superior colliculus (SC) neurons. The cortico-collicular projections from cat anterior ectosylvian sulcus (AES) are derived from its visual, auditory, and somatosensory representations and are critical for multisensory integration. Following tracer injections into each subdivision, 2 types of cortico-collicular axons were observed. Most were categorized as type I and consisted of small-caliber axons traversing long distances without branching, bearing mainly small boutons. The less frequent type II had thicker axons, more complex branching patterns, larger boutons, and more complex terminal boutons. Following combinatorial injections of 2 different fluorescent tracers into defined AES subdivisions, fibers from each were seen converging onto individual SC neurons and indicate that such convergence, like that in the corticothalamic system, is mediated by 2 distinct morphological types of axon terminals. Nevertheless, and despite the conservation of axonal morphologies across different subcortical systems, it is not yet clear if the concomitant physiological attributes described in the thalamus are directly applicable to multisensory integration.

Spatiotemporal architecture of cortical receptive fields and its impact on multisensory interactions

Recent electrophysiology studies have suggested that neuronal responses to multisensory stimuli may possess a unique temporal signature. To evaluate this temporal dynamism, unisensory and multisensory spatiotemporal receptive fields (STRFs) of neurons in the cortex of the cat anterior ectosylvian sulcus were constructed. Analyses revealed that the multisensory STRFs of these neurons differed significantly from the component unisensory STRFs and their linear summation. Most notably, multisensory responses were found to have higher peak firing rates, shorter response latencies, and longer discharge durations. More importantly, multisensory STRFs were characterized by two distinct temporal phases of enhanced integration that reflected the shorter response latencies and longer discharge durations. These findings further our understanding of the temporal architecture of cortical multisensory processing, and thus provide important insights into the possible functional role(s) played by multisensory cortex in spatially directed perceptual processes.

Subthreshold multisensory processing in cat auditory cortex

For multisensory processing to occur, inputs from different sensory modalities must converge onto individual neurons. Traditionally, multisensory neurons have been identified as those which were independently activated by more than one sensory modality. Recently, a different multisensory search paradigm revealed neurons in somatosensory and visual cortex that were activated by only a single modality, whose responses were significantly affected by the presence of a second modality cue. The present experiments recorded neurons in the cat auditory field of the anterior ectosylvian sulcus that also met this criterion, suggesting that subthreshold forms of multisensory processing may represent a general feature of multisensory systems.