Laminar and connectional organization of a multisensory cortex

The transformation of sensory signals as they pass through cortical circuits has been revealed almost exclusively through studies of the primary sensory cortices, for which principles of laminar organization, local connectivity, and parallel processing have been elucidated. In contrast, almost nothing is known about the circuitry or laminar features of multisensory processing in higher order, multisensory cortex. Therefore, using the ferret higher order multisensory rostral posterior parietal (PPr) cortex, the present investigation employed a combination of multichannel recording and neuroanatomical techniques to elucidate the laminar basis of multisensory cortical processing. The proportion of multisensory neurons, the share of neurons showing multisensory integration, and the magnitude of multisensory integration were all found to differ by layer in a way that matched the functional or connectional characteristics of the PPr. Specifically, the supragranular layers (L2/3) demonstrated among the highest proportions of multisensory neurons and the highest incidence of multisensory response enhancement, while also receiving the highest levels of extrinsic inputs, exhibiting the highest dendritic spine densities, and providing a major source of local connectivity. In contrast, layer 6 showed the highest proportion of unisensory neurons while receiving the fewest external and local projections and exhibiting the lowest dendritic spine densities. Coupled with a lack of input from principal thalamic nuclei and a minimal layer 4, these observations indicate that this higher level multisensory cortex shows functional and organizational modifications from the well‐known patterns identified for primary sensory cortical regions. J. Comp. Neurol. 521:1867–1890, 2013. © 2012 Wiley Periodicals, Inc. For multisensory cortex, the laminar distribution of converging extrinsic, unisensory connections favors generation of multisensory properties for L2/3 neurons, as well as L5 neurons via their apical dendrites. Intrinsic translaminar connectivity also contributes to multisensory properties of L5 neurons. Few extrinsic or intrinsic projections reach L6, where most neurons are unisensory. Output targets of L2/3 and 5 are multisensory; output targets of L6 are mostly unisensory areas. These arrangements indicate parallel processing of unisensory and multisensory information within multisensory cortex.