Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat

Mucke, Lennart; Norita, Masao; Benedek, György; Creutzfeldt, O. D.

doi:10.1007/bf00238092

Cited by 202 publications

(104 citation statements)

References 33 publications

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“…This unisensory developmental sequence was predictive of the multisensory chronology, with somatosensory-auditory neurons appearing coincident with the appearance of unisensory auditory neurons and visually responsive multisensory neurons appearing coincident with the appearance of unisensory visual neurons. The appearance and distribution of the different neuronal types in AES was spatially restricted and closely followed the adult functional divisions of AES, with the SIV Stein, 1982, 1983) developing first, the FAES (Clarey and Irvine, 1986) developing second, and the AEV (Mucke et al, 1982;Olson and Graybiel, 1987) developing last.…”

Section: Discussionmentioning

confidence: 85%

The Development of Cortical Multisensory Integration

Wallace

Carriere²,

Perrault³

et al. 2006

J. Neurosci.

117

120

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Although there are many perceptual theories that posit particular maturational profiles in higher-order (i.e., cortical) multisensory regions, our knowledge of multisensory development is primarily derived from studies of a midbrain structure, the superior colliculus. Therefore, the present study examined the maturation of multisensory processes in an area of cat association cortex [i.e., the anterior ectosylvian sulcus (AES)] and found that these processes are rudimentary during early postnatal life and develop only gradually thereafter. The AES comprises separate visual, auditory, and somatosensory regions, along with many multisensory neurons at the intervening borders between them. During early life, sensory responsiveness in AES appears in an orderly sequence. Somatosensory neurons are present at 4 weeks of age and are followed by auditory and multisensory (somatosensory-auditory) neurons. Visual neurons and visually responsive multisensory neurons are first seen at 12 weeks of age. The earliest multisensory neurons are strikingly immature, lacking the ability to synthesize the cross-modal information they receive. With postnatal development, multisensory integrative capacity matures. The delayed maturation of multisensory neurons and multisensory integration in AES suggests that the higher-order processes dependent on these circuits appear comparatively late in ontogeny.

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Section: Discussionmentioning

confidence: 85%

The Development of Cortical Multisensory Integration

Wallace

Carriere²,

Perrault³

et al. 2006

J. Neurosci.

117

120

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show abstract

“…These interconnected areas (Scannell et al 1995; see also Norita et al 1986) contain visual, auditory, and somatosensory neurons (Benedek et al 1983;Stein 1982, 1983;Jiang et al 1994a,b;Mucke et al 1982;Olson and Graybiel 1987;Thompson et al 1963;Toldi and Feher 1984;Wallace et al 1993) that project to the SC (Huerta and Harting 1984;McHaffie et al 1988;Segal and Beckstead 1984;Stein et al 1983) and can affect its neuronal properties Stein 1984, 1986;Meredith and Clemo 1989). The unisensory AES corticocollicular convergence patterns match those received by SC neurons from other sources (Wallace et al 1993), a pattern likely to be paralleled by projections from rLS (Jiang et al 2001).…”

Section: Introductionmentioning

confidence: 96%

Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

Jiang

Jiang²,

Stein³

2006

Journal of Neurophysiology

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ablation disrupts multisensory development in superior colliculus. J Neurophysiol 95: 1380 -1396, 2006. First published November 2, 2005 doi:10.1152/jn.00880.2005. The ability of cat superior colliculus (SC) neurons to synthesize information from different senses depends on influences from two areas of the cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Reversibly deactivating the inputs to the SC from either of these areas in normal adults severely compromises this ability and the SC-mediated behaviors that depend on it. In this study, we found that removal of these areas in neonatal animals precluded the normal development of multisensory SC processes. At maturity there was a substantial decrease in the incidence of multisensory neurons, and those multisensory neurons that did develop were highly abnormal. Their cross-modal receptive field register was severely compromised, as was their ability to integrate cross-modal stimuli. Apparently, despite the impressive plasticity of the neonatal brain, it cannot compensate for the early loss of these cortices. Surprisingly, however, neonatal removal of either AES or rLS had comparatively minor consequences on these properties. At maturity multisensory SC neurons were quite common: they developed the characteristic spatial register among their unisensory receptive fields and exhibited normal adult-like multisensory integration. These observations suggest that during early ontogeny, when the multisensory properties of SC neurons are being crafted, AES and rLS may have the ability to compensate for the loss of one another's cortico-collicular influences so that normal multisensory processes can develop in the SC.

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“…Although the functional role of the AES remains unresolved, the substantial convergence of visual, auditory, and somatosensory inputs suggests that this area plays an important role in the perceptual synthesis of multisensory information. Thus in addition to being divided into three distinct unisensory domains [i.e., the anterior ectosylvian visual area (AEV) (Benedek et al 1988;Mucke et al 1982;Norita et al 1986); the fourth somatosensory cortex (SIV) (Clemo and Stein 1982, 1983, 1984; and the auditory field AES (FAES) (Clarey andIrvine 1986, 1990a,b)], the AES also contains a substantial population of multisensory neurons. These multisensory neurons are clustered at the borders between the major unisensory domains (Wallace et al 2006; but see Jiang et al 1994a,b) and reflect the modalities represented in the neighboring domains (e.g., visual-auditory neurons are of highest incidence at the border between AEV and FAES).…”

Section: Introductionmentioning

confidence: 99%

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

Carriere

Royal²,

Wallace³

2008

Journal of Neurophysiology

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Carriere BN, Royal DW, Wallace MT. Spatial heterogeneity of cortical receptive fields and its impact on multisensory interactions. J Neurophysiol 99: 2357-2368, 2008. First published February 20, 2008 doi:10.1152/jn.01386.2007. Investigations of multisensory processing at the level of the single neuron have illustrated the importance of the spatial and temporal relationship of the paired stimuli and their relative effectiveness in determining the product of the resultant interaction. Although these principles provide a good first-order description of the interactive process, they were derived by treating space, time, and effectiveness as independent factors. In the anterior ectosylvian sulcus (AES) of the cat, previous work hinted that the spatial receptive field (SRF) architecture of multisensory neurons might play an important role in multisensory processing due to differences in the vigor of responses to identical stimuli placed at different locations within the SRF. In this study the impact of SRF architecture on cortical multisensory processing was investigated using semichronic single-unit electrophysiological experiments targeting a multisensory domain of the cat AES. The visual and auditory SRFs of AES multisensory neurons exhibited striking response heterogeneity, with SRF architecture appearing to play a major role in the multisensory interactions. The deterministic role of SRF architecture was tightly coupled to the manner in which stimulus location modulated the responsiveness of the neuron. Thus multisensory stimulus combinations at weakly effective locations within the SRF resulted in large (often superadditive) response enhancements, whereas combinations at more effective spatial locations resulted in smaller (additive/subadditive) interactions. These results provide important insights into the spatial organization and processing capabilities of cortical multisensory neurons, features that may provide important clues as to the functional roles played by this area in spatially directed perceptual processes.

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Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat

Cited by 202 publications

References 33 publications

The Development of Cortical Multisensory Integration

The Development of Cortical Multisensory Integration

Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

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