The mammalian cerebral cortex is innervated by a large number of corticocortical connections. The number of connections makes it difficult to understand the organization of the cortical network. Nonetheless, conclusions about the organization of cortical systems drawn from examining connectional data have often been made in a speculative and informal manner, unsupported by any analytic treatment. Recently, progress has been made toward more systematic ways of extracting organizing principles from data on the network of connections between cortical areas of the monkey. In this article, we extend these approaches to the cortical systems of the cat. We collated information from the neuroanatomical literature about the corticocortical connections of the cat. This collation incorporated 1139 reported corticocortical connections between 65 cortical areas. We have previously used an optimization technique (Scannell and Young, 1993) to analyze this database in order to represent the connectional organization of cortical systems in the cat. Here, we report the connectional database and analyze it in a number of further ways. First, we employed rules from Felleman and Van Essen (1991) to investigate hierarchical relations among the areas. Second, we compared quantitatively the results of the optimization method with the results of the hierarchical method. Third, we examined quantitatively whether simple connection rules, which may reflect the development and evolution of the cortex, can account for the experimentally identified corticocortical connections in the database. The results showed, first, that hierarchical rules, when applied to the cat visual system, define a largely consistent hierarchy. Second, in both auditory and visual systems, the ordering of areas by hierarchical analysis and by optimization analysis was statistically significantly related. Hence, independent analyzes concur broadly in their ordering of areas in the cortical hierarchies. Third, the majority of corticocortical connections, and much of the pattern of connectivity, were accounted for by a simple “nearest-neighbor-or-next-door-but-one” connection rule, which may suggest one of the mechanisms by which the development of cortical connectivity is controlled.

https://www.jneurosci.org/content/jneuro/15/2/1463.full.pdf

Analysis of connectivity in the cat cerebral cortex.

Data on connections between the areas of the cerebral cortex and nuclei of the thalamus are too complicated to analyse with naked intuition. Indeed, the complexity of connection data is one of the major challenges facing neuroanatomy. Recently, systematic methods have been developed and applied to the analysis of the connectivity in the cerebral cortex. These approaches have shed light on the gross organization of the cortical network, have made it possible to test systematically theories of cortical organization, and have guided new electrophysiological studies. This paper extends the approach to investigate the organization of the entire corticothalamic network. An extensive collation of connection tracing studies revealed ~1500 extrinsic connections between the cortical areas and thalamic nuclei of the cat cerebral hemisphere. Around 850 connections linked 53 cortical areas with each other, and around 650 connections linked the cortical areas with 42 thalamic nuclei. Non-metric multidimensional scaling, optimal set analysis and non-parametric cluster analysis were used to study global connectivity and the ‘place’ of individual structures within the overall scheme. Thalamic nuclei and cortical areas were in intimate connectional association. Connectivity defined four major thalamocortical systems. These included three broadly hierarchical sensory or sensory/motor systems (visual and auditory systems and a single system containing both somatosensory and motor structures). The highest stations of these sensory/motor systems were associated with a fourth processing system composed of prefrontal, cingulate, insular and parahippocampal cortex and associated thalamic nuclei (the ‘fronto-limbic system’). The association between fronto-limbic and somato-motor systems was particularly close.

The Connectional Organization of the Cortico-thalamic System of the Cat

Single-neuron activity was recorded in the caudal part of the anterior ectosylvian (AE) cortex of cats that had been deprived of vision for several years by means of binocular lid suture shortly after birth and in normal control animals. Over 300 neurons were tested in each group with auditory, visual, and somatosensory stimuli. We confirmed the existence of an anterior ectosylvian visual area (AEV) in the fundus and ventral bank of the AE sulcus. Neurons in AEV had purely visual responses in normal cats. In visually deprived cats, by contrast, only a minority of cells in this area still responded to visual stimulation. Instead, most cells reacted vigorously to auditory and, to some extent, somatosensory stimuli. The few remaining visual neurons were also driven by auditory or somatosensory stimuli. No increase in the number of unresponsive neurons was found. It appears, therefore, that a cortical region that normally represents visual activity can become driven by auditory or somatosensory activity as a result of visual deprivation. Our results imply that early blindness causes compensatory increases in the amount of auditory cortical representation, possibly by an expansion of nonvisual areas into previously visual territory. In particular, they provide evidence for the existence of neural mechanisms for intermodal compensatory plasticity in the cerebral cortex of young animals. The changes described here may also provide the neural basis for a behavioral compensation for early blindness described elsewhere.

https://www.jneurosci.org/content/jneuro/13/10/4538.full.pdf

Auditory compensation for early blindness in cat cerebral cortex

The majority of multisensory neurons in the cat superior colliculus (SC) are able to synthesize cross-modal cues (e.g., visual and auditory) and thereby produce responses greater than those elicited by the most effective single modality stimulus and, sometimes, greater than those predicted by the arithmetic sum of their modality-specific responses. The present study examined the role of corticotectal inputs from two cortical areas, the anterior ectosylvian sulcus (AES) and the rostral aspect of the lateral suprasylvian sulcus (rLS), in producing these response enhancements. This was accomplished by evaluating the multisensory properties of individual SC neurons during reversible deactivation of these cortices individually and in combination using cryogenic deactivation techniques. Cortical deactivation eliminated the characteristic multisensory response enhancement of nearly all SC neurons but generally had little or no effect on a neuron's modality-specific responses. Thus, the responses of SC neurons to combinations of cross-modal stimuli were now no different from those evoked by one or the other of these stimuli individually. Of the two cortical areas, AES had a much greater impact on SC multisensory integrative processes, with nearly half the SC neurons sampled dependent on it alone. In contrast, only a small number of SC neurons depended solely on rLS. However, most SC neurons exhibited dual dependencies, and their multisensory enhancement was mediated by either synergistic or redundant influences from AES and rLS. Corticotectal synergy was evident when deactivating either cortical area compromised the multisensory enhancement of an SC neuron, whereas corticotectal redundancy was evident when deactivation of both cortical areas was required to produce this effect. The results suggest that, although multisensory SC neurons can be created as a consequence of a variety of converging tectopetal afferents that are derived from a host of subcortical and cortical structures, the ability to synthesize cross-modal inputs, and thereby produce an enhanced multisensory response, requires functional inputs from the AES, the rLS, or both.

https://www.physiology.org/doi/pdf/10.1152/jn.2001.85.2.506

Two Cortical Areas Mediate Multisensory Integration in Superior Colliculus Neurons

Retrograde transport studies have shown that widespread areas of the cerebral cortex project upon the superior colliculus In order to explore the organization of these extensive projections, the anterograde autoradiographic method has been used to reveal the distribution and pattern of corticotectal projections arising from 25 cortical areas In the majority of experiments, electrophysiological recording methods were used to characterize the visual representation and cortical area prior to injection of the tracer

Our findings reveal that seventeen of the 25 cortical areas project upon some portion of the superficial layers (stratum zonale, stratum griseum superficiale, and stratum opticum, SO) These cortical regions include areas 17, 18, 19, 20a, 20b, 21a, 21b, posterior suprasylvian area (PS), ventral lateral suprasylvian area (VLS), posteromedial lateral suprasylvian area (PMLS), anteromedial lateral suprasylvian area (AMLS), anterolateral lateral suprasylvian area (ALLS), posterolateral lateral suprasylvian area (PLLS), dorsolateral lateral suprasyvian area (DLS), periauditory cortex, cingulate cortex, and the visual portion of the anterior ectosylvian sulcus While some of these corticotectal projections target all superficial laminae and sublaminae, others are more discretely organized in their laminar-sublaminar distribution Only the corticotectal projections arising from areas 17 and 18 are exclusively related to the superficial layers The remaining 15 pathways innervate both the superficial and intermediate and/or deep layers

The large intermediate gray layer (stratum griseum intermedium; SGI) receives projections from almost every cortical area; only areas 17 and 18 do not project ventral to SO All corticotectal projections to SGI vary in their sublaminar distribution and in their specific pattern of termination The majority of these projections are periodic, or patchy, and there are elaborate (double tier, bridges, or streamers) modes of distribution We have attempted to place these findings into a conceptual framework that emphasizes that the SGI consists of sensory and motor domains, both of which contain a mosaic of connectionally distinct afferent compartments (Illing and Graybiel, '85, Neuroscience 14:455–482; Harting and Van Lieshout, '91, J Comp Neurol 305:543–558)

Corticotectal projections to the layers ventral to SGI, (stratum album intermediale, stratum griseum profundum, and stratum album profundum) arise from thirteen cortical areas While an organizational plan of these deeper projections is not readily apparent, the distribution of several corticotectal inputs reveals some connectional parcellation

Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas.

We have previously described a visual area situated in the cortex surrounding the deep infolding of the anterior ectosylvian sulcus of the cat (Mucke et al. 1982). Using orthograde and retrograde transport methods we now report anatomical evidence that this anterior ectosylvian visual area (AEV) is connected with a substantial number of both cortical and subcortical regions. The connections between AEV and other cortical areas are reciprocal and, at least in part, topographically organized: the rostral AEV is connected with the bottom region of the presylvian sulcus, the lower bank of the cruciate sulcus, the rostral part of the ventral bank of the splenial sulcus, the rostral portion of the lateral suprasylvian visual area (LS) and the lateral bank of the posterior rhinal sulcus; the caudal AEV is connected with the bottom region of the presylvian sulcus, the caudal part of LS, the ventral part of area 20 and the lateral bank of the posterior rhinal sulcus. Subcortically, AEV has reciprocal connections with the ventral medial thalamic nucleus (VM), with the medial part of the lateralis posterior nucleus (LPm), as well as with the lateralis medialis-suprageniculate nuclear (LM-Sg) complex. These connections are also topographically organized with more rostral parts of AEV being related to more ventral portions of the LPm and LM-Sg complex. AEV also projects to the caudate nucleus, the putamen, the lateral amygdaloid nucleus, the superior colliculus, and the pontine nuclei. It is concluded that AEV is a visual association area which functionally relates the visual with both the motor and the limbic system and that it might play a role in the animal's orienting and alerting behavior.

B. Albowitz

Papers

Connections of the anterior ectosylvian visual area (AEV)