Abstract
Topographic representation of the receptor surface is a fundamental feature of sensory cortical organization. This is imparted by the thalamus, which relays information from the periphery to the cortex. To better understand the rules governing thalamocortical connectivity and the origin of cortical maps, we used in vivo two-photon calcium imaging to characterize the properties of thalamic axons innervating different layers of mouse auditory cortex. Although tonotopically organized at a global level, we found that the frequency selectivity of individual thalamocortical axons is surprisingly heterogeneous, even in layers 3b/4 of the primary cortical areas, where the thalamic input is dominated by the lemniscal projection. We also show that thalamocortical input to layer 1 includes collaterals from axons innervating layers 3b/4 and is largely in register with the main input targeting those layers. Such locally varied thalamocortical projections may be useful in enabling rapid contextual modulation of cortical frequency representations.
Highlights
The vast majority of ascending sensory information reaches the cortex via the thalamus
Across different anesthetic states and different strains of mice, we found that the tuning of neighboring boutons is surprisingly heterogeneous, that frequency gradients are apparent at a large spatial scale only, and that thalamic inputs to cortical layers 1 and 3b/4 share a coarse tonotopic organization
We demonstrate that this organization, which provides a potential basis for the broad spectral integration and experience-dependent plasticity that are characteristic features of the tuning properties of auditory cortical neurons, reflects almost exclusively the properties of the lemniscal thalamocortical projection originating in the ventral division of the medial geniculate body (MGB)
Summary
The vast majority of ascending sensory information reaches the cortex via the thalamus. Most of the brain's auditory neurons, including those in the medial geniculate body (MGB) of the thalamus, are tuned to sound frequency and their spatial arrangement reflects the tonotopic organization established by the biomechanical properties of the cochlea. The opportunity to image the activity of large populations of neurons at single-cell resolution in the mouse auditory cortex (Bandyopadhyay et al, 2010; Issa et al, 2014; Rothschild et al, 2010; Winkowski and Kanold, 2013) has questioned the smooth tonotopic organization revealed with microelectrode recordings (Guo et al, 2012; Hackett, 2011; Stiebler et al, 1997) or low-resolution imaging methods (Horie et al, 2013; Moczulska et al, 2013; Tsukano et al, 2016). The current view holds that neurons in the main thalamorecipient layers 4 and
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