Patterns of sensory intermodality relationships in the cerebral cortex of the rat

Abstract

Patterns of connections underlying cross-modality integration were studied by injecting distinguishable, retrograde tracers (Fluoro-Gold and diamidino yellow) in pairwise manner into different sensory representations (visual, somatosensory, and auditory) in the cerebral cortex of the rat. In agreement with previous single tracer studies, our results indicate that the central core of sensory areas receives projections mainly from a set of association areas located in a ringlike fashion along the margin of the cortical mantle. The visual cortex received projections from areas 48/49, area 29d, posterior agranular medial cortex (AGm), area 11, area 13, and area 35. All these areas were also connected to the auditory cortex with the exception of areas 29d and AGm. However, lateral to area 29d and posterior AGm, a band of neurons projecting to the auditory cortex was present. Somatosensory cortex was connected mainly with the more anterior aspect of the hemisphere, which included primary motor area, area 11, and area 13. The patterns of intermodality relationships revealed in the present study were of two main categories. In the anterior and lateral areas, an intermingling of cells projecting to different sensory modalities was observed. In contrast, in areas located along the medial aspect of the hemisphere, cells connected to different sensory modality representations tended to be segregated from each other. Postsubicular cortex (areas 48/49) contained both intermingled and segregated groups of cells. The incidence of clearly identified double-labeled cells concurrently projecting to two different sensory representations was extremely rare. These patterns may form a substrate for different levels of cross-modal sensory integration in the rat cortex.

The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function

“…A return projection to the auditory cortex from the perirhinal cortex has also been described (Paperna and Malach, 1991); perirhinal projections terminating mainly in layers I-III and VI of the auditory association cortices (Agster and Burwell, 2009). Return projections from the perirhinal cortex to the secondary auditory areas have also been reported (Paperna and Malach, 1991); projections from the middle layers of the caudal region of area 36 terminate mainly in the superficial and middle layers of Te2 and in the superficial layers of Te3 (Shi and Cassell, 1999). However, Shi and Cassell's (1999) definition of the perirhinal cortex differs from our definition and some of these projections may actually be postrhinal in origin.…”

“…In keeping with the perirhinal cortex's role as an association area, it receives input from a number of sensory or associative areas, namely the parietal, insular, ventral temporal association, piriform, periamygdaloid, visual and auditory cortices (Deacon et al, 1983;Paperna and Malach, 1991;Burwell and Amaral, 1998b). The first three areas of cortex listed are both associative in nature; the parietal cortex acts as a site for associating perceptual stimuli (Save and Poucet, 2009), spatial representation Poucet, 2000, 2009;Nitz, 2009) and may act as an interface between attention and learning during working memory (Bucci, 2009), the insular cortex has many different sensory and associative functions attributed to it (Rodgers et al, 2008) and the ventral temporal association cortex is involved in integrating separate sensory modalities (Bai et al, 2004).…”

“…However, light labelling in the caudal perirhinal cortex has been reported following injection of the anterograde tracer Phaseolus vulgaris leucoagglutinin into the primary visual cortex (McDonald and Mascagni, 1996) and electrophysiological stimulation of the primary visual cortex has been shown to evoke fEPSPs in the perirhinal cortex (Naber et al, 2000). The perirhinal cortex shows a greater connectivity with the visual association areas compared to the primary visual cortex (Paperna and Malach, 1991;McDonald and Mascagni, 1996); the projection from the visual association cortex originates in layers II, V and VI and terminates only in the caudal region of area 36 (Burwell and Amaral, 1998b;Agster and Burwell, 2009). …”

“…There are also an input to the perirhinal cortex from the secondary auditory areas Te2 and Te3; the ventral regions of Te2 and Te3 project to the caudal region of area 36 (Arnault and Roger, 1990;Shi and Cassell, 1997). A return projection to the auditory cortex from the perirhinal cortex has also been described (Paperna and Malach, 1991); perirhinal projections terminating mainly in layers I-III and VI of the auditory association cortices (Agster and Burwell, 2009). Return projections from the perirhinal cortex to the secondary auditory areas have also been reported (Paperna and Malach, 1991); projections from the middle layers of the caudal region of area 36 terminate mainly in the superficial and middle layers of Te2 and in the superficial layers of Te3 (Shi and Cassell, 1999).…”

“…As described in Sections 2.2 and 2.3, there are different distributions of neuron types in the various layers of the perirhinal cortex and where the various projections to and from the perirhinal cortex begin or terminate may be dependent on what cell types (and therefore what layers) are involved. An interesting observation by Paperna and Malach (1991) was the intermingling of perirhinal efferents to the visual and auditory cortices. They suggest that this intermingling may allow for cross talk between the different sensory modalities, reinforcing the idea of the perirhinal cortex being an association area.…”