Complementary control of sensory adaptation by two types of cortical interneurons

Abstract

Reliably detecting unexpected sounds is important for environmental awareness and survival. By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA). The majority of neurons in the primary auditory cortex exhibit SSA, yet little is known about the underlying cortical circuits. We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons. Parvalbumin-positive interneurons (PVs) amplify SSA by providing non-specific inhibition: optogenetic suppression of PVs led to an equal increase in responses to frequent and rare tones. In contrast, somatostatin-positive interneurons (SOMs) selectively reduce excitatory responses to frequent tones: suppression of SOMs led to an increase in responses to frequent, but not to rare tones. A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.DOI: http://dx.doi.org/10.7554/eLife.09868.001

Contextual modulation of sound processing in the auditory cortex

“…Curiously, this phenomenon results in frequency hyperacuity in single neurons which matches the psychophysical acuity of untrained humans in a frequency discrimination task [38]. Converging evidence suggests that SSA is mediated through a combination of feedforward synaptic depression and intra-cortical inhibition [27,39]. Parvalbumin-positive (PV) and somatostatin-positive (SOM) interneurons differentially contribute to SSA, with PVs providing non-specific inhibition to the frequent and rare tones, while SOMs selectively inhibit frequent tones in a manner that increases over time [27].…”

“…Sensitivity to temporal context is important for identifying auditory objects, allowing sequences of auditory stimuli to be perceptually grouped or separated based on their temporal properties [24,25] or for detecting novel or rare sounds by decreasing responsivity to redundant sounds [26,27]. …”

“…Stimulus specific adaptation (SSA) is one such phenomenon, in which neurons reduce their response to a tone frequently repeated over several seconds, but do not suppress their response to a rarely presented tone of a different frequency [27,33–37]. SSA typically occurs over the course of several seconds [35–37] and can be elicited by tones whose frequency difference is an order of magnitude smaller than typical cortical and auditory nerve tuning widths [33,36].…”

“…Converging evidence suggests that SSA is mediated through a combination of feedforward synaptic depression and intra-cortical inhibition [27,39]. Parvalbumin-positive (PV) and somatostatin-positive (SOM) interneurons differentially contribute to SSA, with PVs providing non-specific inhibition to the frequent and rare tones, while SOMs selectively inhibit frequent tones in a manner that increases over time [27]. Taken together, these findings outline a key role for interneuron-mediated synaptic inhibition in adaption to temporal context, providing a neural mechanism by which sound sequences and temporal events are encoded in auditory cortex.…”

Auditory cortex interneuron development requires cadherins operating hair-cell mechanoelectrical transduction

“…These difficulties might be related to the involvement of PV interneurons in the experience-driven neural plasticity underlying AC maturation (8,54) and the temporal precision of sound detection critical for speech perception (55). The shaping of the perception of several acoustic features throughout life, including frequency discrimination acuity (56) and the detection of unexpected sounds, also involves PV interneurons of the AC (57).…”