Laminar Transformation of Frequency Organization in Auditory Cortex

Abstract

The mammalian neocortex is a six-layered structure organized into radial columns. Within sensory cortical areas, information enters in the thalamorecipient layer and is further processed in supra- and infra-granular layers. Within the neocortex, topographic maps of stimulus features are present, but whether topographic patterns of active neurons change between laminae is unknown. Here, we used in vivo two-photon Ca2+ imaging to probe the organization of the mouse primary auditory cortex and show that the spatial organization of neural response properties (frequency tuning) within the thalamorecipient layer (L3b/4) is more homogeneous than in supragranular layers (L2/3). Moreover, stimulus-related correlations between pairs of neurons are higher in the thalamorecipient layer whereas stimulus-independent trial-to-trial covariance is higher in supragranular neurons. These findings reveal a transformation of sensory representations that occurs between layers within the auditory cortex, which could generate sequentially more complex analysis of the acoustic scene incorporating a broad range of spectro-temporal sound features.

Local versus global scales of organization in auditory cortex

“…The third type of evidence for local order in A1 comes from recent in vivo 2-photon Ca 2+ imaging of layer 4 and layer 2/3 neurons in the same animal. This study demonstrated directly that the representation of frequency is much more homogeneous in layer 4 than in layer 2/3 [75] (Fig. 2b).…”

“…First, while responses of simultaneously imaged cells were heterogeneous, neurons did show high noise correlation suggesting that they might form interconnected networks [65, 73, 74]. These noise correlations decreased with distance between neurons, with a spatial scale of about 100 microns [65, 75] (see also [76]), suggesting that neuronal interactions are organized within anatomical columns. Second, different Ca 2+ dyes have different affinity for Ca 2+ and thus can report different aspects of the neural response.…”

Harmonic template neurons in primate auditory cortex underlying complex sound processing

“…A previous study in awake marmosets found a high proportion of combination-selective, nontoneresponsive, and low spontaneous-firing neurons at superficial cortical depths in A1 (49). A two-photon imaging study showed that A1 neurons in layer IV respond more strongly to pure tones than neurons in upper layers (56). To fully understand the hierarchical auditory processing of harmonic information, it will be important to investigate the circuitry basis of HTNs and their connectivity to other neurons in auditory cortex in future studies.…”

Multiscale Optical Ca2+ Imaging of Tonal Organization in Mouse Auditory Cortex

“…Perhaps, highly active and tonotopically organized neurons predominate in layer IV, while weakly responding and poorly tuned neurons prevail in superficial layers II/III of cortex. A recent two-photon study argues for such a scenario via explicit comparison of responses in layers IV and II/III (Winkowski and Kanold, 2013). However, the majority of neurons investigated in the present study are from layers II/III (Figure S1Q), which nonetheless exhibit strong tonotopicity (Figures 6A–C).…”