Abstract
Corticofugal projections outnumber subcortical input projections by far. However, the specific role for signal processing of corticofugal feedback is still less well understood in comparisonto the feedforward projection. Here, we lesioned corticothalamic (CT) neurons in layers V and/or VI of the auditory cortex of Mongolian gerbils by laser-induced photolysis to investigate their contribution to cortical activation patterns. We have used laminar current-source density (CSD) recordings of tone-evoked responses and could show that, particularly, lesion of CT neurons in layer VI affected cortical frequency processing. Specifically, we found a decreased gain of best-frequency input in thalamocortical (TC)-recipient input layers that correlated with the relative lesion of layer VI neurons, but not layer V neurons. Using cortical silencing with the GABAa-agonist muscimol and layer-specific intracortical microstimulation (ICMS), we found that direct activation of infragranular layers recruited a local recurrent cortico-thalamo-cortical loop of synaptic input. This recurrent feedback was also only interrupted when lesioning layer VI neurons, but not cells in layer V. Our study thereby shows distinct roles of these two types of CT neurons suggesting a particular impact of CT feedback from layer VI to affect the local feedforward frequency processing in auditory cortex.
Highlights
Being positioned at the nexus between the ascending subcortical and descending higher-cortical auditory pathway, the auditory cortex (ACx) is central for auditory processing and behavior (Scheich et al, 2007; Schreiner and Winer, 2007; Budinger et al, 2008; Sharpee et al, 2011; King et al, 2018)
After photolytic lesioning of auditory CT projection neurons in Mongolian gerbils we performed in vivo multichannel recordings of local field potentials (LFP) and laminar current-source density (CSD) distributions from primary ACx to investigate the impact of the lesions on auditory cortical processing at the circuit level using acoustic and electrical stimulation
Whereas lesion of CT neurons in layer V had no or only moderate effects on tone or ICMSevoked cortical processing, lesion of CT neurons in layer VI led to layer-specific changes of the tone-evoked spatiotemporal cortical activity profile with a reduced input gain for preferred frequency input
Summary
Being positioned at the nexus between the ascending subcortical and descending higher-cortical auditory pathway, the auditory cortex (ACx) is central for auditory processing and behavior (Scheich et al, 2007; Schreiner and Winer, 2007; Budinger et al, 2008; Sharpee et al, 2011; King et al, 2018). Ferrets whose layer VI CT neurons of the ACx had been selectively lesioned by means of a chromophoretargeted laser photolysis showed impaired perceptual grouping of harmonics—one of the key cues in the perception of complex sounds (Homma et al, 2017) We applied this method in the Mongolian gerbil (Meriones unguiculatus) to investigate the contributions of CT neurons to acoustically and electrically evoked population activity patterns of primary ACx (field AI) as revealed by currentsource density (CSD) analysis (Happel et al, 2010). We could demonstrate that intact CT feedback from layer VI is crucial for this electrically evoked columnar population pattern: Selective apoptosis of CT neurons in layer VI diminished this direct ICMS-evoked columnar activation significantly This finding confirms our hypothesis that infragranular microstimulation activates a fast-acting recurrent CT loop via the ventral part of the MBG (MGv; Happel et al, 2014). Our study thereby shows that layer VI CT neurons affect the columnar frequency processing in ACx through a frequency-specific gain in TC-recipient layers
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