Medial geniculate body and primary auditory cortex differentially contribute to striatal sound representations

Abstract

The dorsal striatum has emerged as a key region in sensory-guided, reward-driven decision making. A posterior sub-region of the dorsal striatum, the auditory striatum, receives convergent projections from both auditory thalamus and auditory cortex. How these pathways contribute to auditory striatal activity and function remains largely unknown. Here we show that chemogenetic inhibition of the projections from either the medial geniculate body (MGB) or primary auditory cortex (ACx) to auditory striatum in mice impairs performance in an auditory frequency discrimination task. While recording striatal sound responses, we find that transiently silencing the MGB projection reduced sound responses across a wide-range of frequencies in striatal medium spiny neurons. In contrast, transiently silencing the primary ACx projection diminish sound responses preferentially at the best frequencies in striatal medium spiny neurons. Together, our findings reveal that the MGB projection mainly functions as a gain controller, whereas the primary ACx projection provides tuning information for striatal sound representations.

Single cell plasticity and population coding stability in auditory thalamus upon associative learning

“…We found similar proportions of CS and US plastic neurons in first order cortex-projecting and higher order areas of MGB. Higher order areas of MGB are more broadly-projecting areas of auditory thalamus and target among others large parts of auditory cortex as well as striatum and amygdala (Chen et al, 2019;Jones, 1998;Kimura et al, 2003;Smith et al, 2019). Given the amygdala's prominent role in associative fear learning we hypothesized that CS and US plastic neurons are specifically enriched in MGB→BLA projection neurons when compared to the total population including less plastic MGBv neurons Weinberger, 1991b, 1992).…”

“…Surprisingly, we found that the proportion of plastic neurons was not enhanced in amygdala-projecting neurons and was similar to the proportion of plastic neurons in the total MGB population. This lack of enrichment of neurons with dedicated functions in associative learning suggests that the MGB→BLA pathway is most likely not a labelled line, but that MGB potentially propagates experience-dependent changes of neuronal activity in associative fear learning to a wider brain network, including auditory cortex and striatum (Chen et al, 2019). This is reminiscent of recent findings that heterogenous behaviour-related neural activity of projection neurons of a given brain area is broadcast simultaneously and in parallel to different downstream targets irrespective of the output pathway (Gründemann et al, 2019;Weglage et al, 2020).…”

“…While the population code of the amygdala stabilizes "fear hijacking" of the sensory representation, MGB exhibits transient changes in population level encoding, which provides a clean slate for future perception that is unaffected by a valence bias. Nevertheless, the transient population level changes during fear conditioning in MGB might be crucial to guide long term population level changes in the amygdala or other downstream areas upon associative learning (Chen et al, 2019;Grewe et al, 2017;Zhang and Li, 2018).…”

“…Higher order MGBm neurons project to different output targets including primary and secondary auditory cortex, striatum and the basolateral amygdala (Chen et al, 2019;Kimura et al, 2003;Kwon et al, 2014;Smith et al, 2019). Enrichment of plastic neurons in the MGB→BLA pathway might be crucial for fear learning, given BLA's key role in aversive memory formation (LeDoux, 2000).…”

Learning-related population dynamics in the auditory thalamus

“…In addition, a large body of evidence indicates that the medial MGB is involved in auditory fear conditioning, by providing fast, less refined auditory information to the lateral amygdala (Han et al, 2008; Herry and Johansen, 2014; Maren and Quirk, 2004; Quirk et al, 1995; Romanski and LeDoux, 1992; Weinberger, 2011), an indication of experience dependent synaptic plasticity in the MGB. Nevertheless, whether MGB encodes learning-related modulation beyond the fear system, remains unknown (Chen et al, 2019; Jaramillo et al, 2014). To study learning related modulations in the MGB, we chronically imaged MGB population responses to sounds as mice learned a go/no-go auditory discrimination task.…”