Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons

Abstract

The organization of layer VI in cat primary auditory cortex (AI) was studied in mature specimens. Golgi‐impregnated neurons were classified on the basis of their dendritic and somatic form. Ipsilateral and contralateral projection neurons and the corticogeniculate cells of origin were labeled with retrograde tracers and their profiles were compared with the results from Golgi studies. Layer VI was divided into a superficial half (layer VIa) with many pyramidal neurons and a deeper part (layer VIb) that is dominated by horizontal cells. Nine types of neuron were identified; four classes had subvarieties. Classical pyramidal cells and star, fusiform, tangential, and inverted pyramidal cells occur. Nonpyramidal neurons were Martinotti, multipolar stellate, bipolar, and horizontal cells. This variety of neurons distinguished layer VI from other AI layers. Pyramidal neuron dendrites contributed to the vertical, modular organization in AI, although their apical processes did not project beyond layer IV. Their axons had vertical, intrinsic processes as well as corticofugal branches. Horizontal cell dendrites extended laterally up to 700 μm and could integrate thalamic input across wide expanses of the tonotopic domain. Connectional experiments confirmed the sublaminar arrangement seen in Nissl material. Commissural cells were concentrated in layer VIa, whereas corticocortical neurons were more numerous in layer VIb. Corticothalamic cells were distributed more equally. The cytological complexity and diverse connections of layer VI may relate to a possible role in cortical development. Layer VI contained most of the neuronal types found in other layers in AI, and these cells form many of the same intrinsic and corticofugal connections that neurons in other layers will assume in adulthood. Layer VI, thus, may play a fundamental ontogenetic role in the construction and early function of the cortex. J. Comp. Neurol. 404:332–358, 1999. © 1999 Wiley‐Liss, Inc.

Orexin-dependent activation of layer VIb enhances cortical network activity and integration of non-specific thalamocortical inputs

“…Layer VIb neurons predominantly project cortico-cortically towards ipsilateral or contralateral targets (Prieto and Winer 1999;Arimatsu et al 2003), but their output pattern to other layers is controversial. Indeed, some studies suggest that layer VIb projections are confined to infragranular layers (Zhang and Deschenes 1998;Mercer et al 2005), whereas others indicate that these projections reach supragranular layers (Valverde et al 1989;Usrey and Fitzpatrick 1996;Hirsch et al 1998;Clancy and Cauller 1999;Marx and Feldmeyer 2013), and further discrepancies exist between these reports regarding projections to individual layers.…”

“…Layer VI sends callosal projections to the contralateral cortex (Code and Winer 1985;Prieto and Winer 1999). To test the functional contribution of sublayer VIb to these projections, we prepared coronal slices preserving commissural axons and both hemispheres (see Materials and methods).…”

“…Among these nuclei, those of the thalamic midline are sensitive to orexins and may thus play a critical role in cortical arousal (Bayer et al 2002). Layer VIa is a key component of the cortico-thalamic feedback, whereas layer VIb primarily sends intracortical projections (Usrey and Fitzpatrick 1996;Hirsch et al 1998;Zhang and Deschenes 1998;Prieto and Winer 1999;Clancy and Cauller 1999;Arimatsu et al 2003;Mercer et al 2005;Jones 2007;Marx and Feldmeyer 2013). This pattern of input-output connections and sensitivity to wake-promoting neurotransmitters suggests that layer VIb may act as an intracortical relay of information on vigilance states.…”

Involvement of the Thalamocortical Loop in the Spontaneous Switching of Percepts in Auditory Streaming

“…In monkeys, inputs from the ventral division of the MGB are projected to layers III and IV in the primary auditory area (core region), whereas those from the dorsal division of the MGB are projected to layers I, II, V, and VI in the secondary auditory area (belt and parabelt regions) (Winer, 1985;Villa et al, 1991). The MGB receives feedback from layers V and VI of the AC (Prieto and Winer, 1999;Winer and Prieto, 2001). The structure of the auditory system in humans appears to be similar to that in monkeys (Rivier and Clarke, 1997;Rademacher et al, 2001;Sweet et al, 2005).…”

Dissecting Neuronal Circuits: Analysis of Basket Cell-like Interneurons in Cortical Layer 6

“…Significant effort has been made to group these neurons based on their morphologies Chen, Abrams, Pinhas, & Brumberg, 2009;Ferrer, Fabregues, & Condom, 1986;Kumar & Ohana, 2008;Markram et al, 2015;O'Leary, 1941;Prieto & Winer, 1999;Tömböl, 1984). L6 interneurons characterized as "fast spiking" are thought to have a critical role in brain functions (Bortone, Olsen, & Scanziani, 2014;Cruikshank, Urabe, Nurmikko, & Connors, 2010;Olsen, Bortone, Adesnik, & Scanziani, 2012).…”