M. Alex Meredith

Spatial factors determine the activity of multisensory neurons in cat superior colliculus

The responses of a neuron to stimuli from one sensory modality can be profoundly influenced by inputs from other sensory modalities. The present experiments demonstrate that the nature and the magnitude of these multisensory interactions depend on the positions of the stimuli in relation to their respective receptive fields. The spatial rules governing these interactions underscore the significance of the alignment of sensory maps in the brain.

Integration of multiple sensory modalities in cat cortex

SummaryThe results of this study show that the different receptive fields of multisensory neurons in the cortex of the cat anterior ectosylvian sulcus (AES) were in spatial register, and it is this register that determined the manner in which these neurons integrated multiple sensory stimuli. The functional properties of multisensory neurons in AES cortex bore fundamental similarities to those in other cortical and subcortical structures. These constancies in the principles of multisensory integration are likely to provide a basis for spatial coherence in information processing throughout the nervous system.

Neurons and behavior: the same rules of multisensory integration apply.

Combinations of different sensory cues (e.g. auditory and visual) that are coincident in space enhance the responses of multisensory superior colliculus neurons, while the responses of these same neurons are depressed if the stimuli are separated in space. Using a behavioral paradigm modeled after that used in physiological studies, the present experiments demonstrate that the rules governing multisensory integration at the level of the single neuron also predict the responses to these stimuli in the intact behaving animal.

Chapter 8 The visually responsive neuron and beyond: multisensory integration in cat and monkey

Publisher Summary The cat superior colliculus neuron is a major site for the convergence and integration of multisensory information. It is only one of many central nervous system sites in many species where information from several modalities converges. Single cells in cat LS (lateral suprasylvian) and AES (anterior ectosylvian sulcus) and in monkey IPS (intraparietal sulcus) and STS (superior temporal sulcus) were examined. Although the spatial, temporal, and multiplicative characteristics of multisensory integration were most closely examined in cat cortex, all of the observations in monkey were consistent with those described in cat. The multisensory receptive fields of a single neuron overlapped one another in space, such that sensory stimuli that were in close spatial register fell within their excitatory receptive fields and enhanced the neurons activity; spatially disparate stimuli produced either no interaction or depressed responses. The rules of multisensory integration evident at the level of the single neuron are also consistent with studies of intact behaving animals. The attentive and orientation responses cats make to visual and auditory stimuli were predictable based on the reactions of superior colliculus neurons to these stimuli. The data indicate that the visual responses of many neurons, whether in the superior colliculus or cortex, represent only one facet of their sensory coding capabilities.

Chemoarchitecture of GABAergic neurons in the ferret superior colliculus.

γ‐Aminobutyric acid (GABA)ergic neurons are thought to play a key role both in visual processing and in the complex sensory‐motor transformations that take place in the mammalian superior colliculus. To understand the organization of GABAergic neurons in the ferret superior colliculus, we applied antisera to several markers of GABAergic function, including GABA, two isoforms of its synthetic enzyme glutamic acid decarboxylase (GAD‐65 and GAD‐67), and the GABA transporter, GAT‐1. We also applied antisera to several calcium binding proteins (calbindin [CB], calretinin [CR], and parvalbumin [PV]) and neuronal nitric oxide synthase (NOS), chemical markers that colocalize with GABA in some areas of the central nervous system. The distribution of GABAergic neurons in the ferret is similar to that of other mammalian species. GABAergic neurons in the ferret superior colliculus were small, morphologically diverse, and widely distributed throughout all layers of the colliculus. As has been shown in other mammalian species, neurons expressing PV, CB, CR, and NOS were differentially distributed in layers and patches throughout the ferret colliculus. None of these markers, however, showed a distribution that mirrored that of GABAergic neurons. Furthermore, few GABAergic neurons colocalized these neurochemical markers. Only 14% of GABAergic neurons in the superficial layers and 18% of neurons in the deeper layers colocalized PV, 14% of GABAergic neurons in the superficial layers and 10% in the deeper layers colocalized CB, and only 1% of GABAergic neurons in both the superficial and deep layers colocalized nitric oxide synthase. Thus, the arrangement of GABAergic neurons in the ferret superior colliculus is broadly distributed and is distinct from other recognized organizational patterns in the superior colliculus. J. Comp. Neurol. 452:334–359, 2002.

The frontal eye fields target multisensory neurons in cat superior colliculus.

Abstract While sensory corticotectal connections have received considerable attention, relatively little is known about the nature of superior colliculus neurons that receive input from the cortical frontal eye fields. The present experiments used microstimulation of indwelling electrodes in the frontal eye fields and single-unit recording in the superior colliculus to demonstrate that frontal afferents preferentially terminate on multisensory neurons in the colliculus. Furthermore, the medial and lateral subdivisions of the cat frontal eye fields access physiologically distinct populations of multisensory collicular neurons. Specifically, the medial subdivision preferentially activates neurons with visual and auditory sensory responses located medial within the colliculus, while the lateral subdivision preferentially activates collicular neurons with visual and somatosensory responses found more laterally. These data support reports distinguishing the medial and lateral subdivisions of the frontal eye fields in the cat and suggest that signals from each may route separately through the colliculus to induce or coordinate different components of gaze control.

Cortico-cortical relations of cat somatosensory areas SIV and SV.

Sensory cortex is characterized by multiple representations of a given modality which are generally highly interconnected and hierarchically arranged. The cat cerebral cortex contains at least five major areas dedicated to somatosensory processing, yet aside from areas SI and SII, little is known regarding the interconnectivity of the other, higher-level regions, such as SIV and SV. Therefore, this investigation examined the anatomical relationship of somatosensory areas SIV and SV to each other. In adult cats, wheatgerm agglutinin–horseradish peroxidase (WGA-HRP) injected into SIV produced retrogradely labeled neurons in SV in a bilaminar pattern. When biotinylated dextran amine (BDA) was injected into SV, orthogradely labeled axon terminals were found in SIV across all laminae but predominated in supragranular locations. In the reciprocal direction, neurons located in both the supra- and infragranular layers of SIV projected across all laminae of SV, but also in a manner that favored the supragranular layers. Because local inhibitory circuits are critical for specific somatosensory response properties, the distribution of GABA-ergic neurons and their co-localized markers calbindin (CB), calretinin (CR) and parvalbumin (PV) was also compared for SIV and SV using immunocytochemical techniques. Although fundamental differences in laminar arrangement were observed between the different GABA-ergic subtypes, the distribution for each subtype was essentially the same in both SIV and SV. Collectively, these connectional, cytoarchitectonic and organizational similarities indicate that SIV and SV are reciprocally connected and share many somatosensory processing and connectional features.Sensory cortex is characterized by multiple representations of a given modality which are generally highly interconnected and hierarchically arranged. The cat cerebral cortex contains at least five major areas dedicated to somatosensory processing, yet aside from areas SI and SII, little is known regarding the interconnectivity of the other, higher-level regions, such as SIV and SV. Therefore, this investigation examined the anatomical relationship of somatosensory areas SIV and SV to each other. In adult cats, wheatgerm agglutinin-horseradish peroxidase (WGA-HRP) injected into SIV produced retrogradely labeled neurons in SV in a bilaminar pattern. When biotinylated dextran amine (BDA) was injected into SV, orthogradely labeled axon terminals were found in SIV across all laminae but predominated in supragranular locations. In the reciprocal direction, neurons located in both the supra- and infragranular layers of SIV projected across all laminae of SV, but also in a manner that favored the supragranular layers. Because local inhibitory circuits are critical for specific somatosensory response properties, the distribution of GABA-ergic neurons and their co-localized markers calbindin (CB), calretinin (CR) and parvalbumin (PV) was also compared for SIV and SV using immunocytochemical techniques. Although fundamental differences in laminar arrangement were observed between the different GABA-ergic subtypes, the distribution for each subtype was essentially the same in both SIV and SV. Collectively, these connectional, cytoarchitectonic and organizational similarities indicate that SIV and SV are reciprocally connected and share many somatosensory processing and connectional features.