Single cell plasticity and population coding stability in thalamic circuits upon associative learning.

Cortical and limbic brain areas are regarded as centers for learning. However, how thalamic
sensory relays participate in plasticity upon associative learning, yet support stable long-term
sensory coding remains unknown. Using a miniature microscope imaging approach, we
monitor the activity of populations of auditory thalamus (medial geniculate body) neurons in
freely moving mice upon fear conditioning. We find that single cells exhibit mixed selectivity
and heterogeneous plasticity patterns to auditory and aversive stimuli upon learning that is
independent from cortical feedback. We identified neurons in medial geniculate body that
encode for the upcoming behavior of the animal. Cholinergic inputs to the medial geniculate
body modulate the associative learning. The plasticity and neuronal responses to the different
stimuli are conserved in amygdala-projecting medial geniculate body neurons but there is no
enhanced plasticity in these cells. Activity in auditory thalamus to amygdala-projecting neurons
stabilizes single cell plasticity in the total medial geniculate body population and is necessary
for fear memory consolidation. In contrast to individual cells, population level encoding of
auditory stimuli remained stable across days. Our data identifies auditory thalamus as a site
for complex neuronal plasticity in fear learning upstream of the amygdala that is in an ideal
position to drive plasticity in cortical and limbic brain areas. These findings suggest that medial
geniculate body’s role goes beyond a sole relay function by balancing experience-dependent,
diverse single cell plasticity with consistent ensemble level representations of the sensory
environment to support stable auditory perception with minimal affective bias.