Stimulus-specific adaptation occurs in the auditory thalamus

Abstract

Neurons in the primary auditory cortex respond less strongly to a commonly occurring "standard" tone than to the same tone when it is rare or "deviant." This phenomenon, called "stimulus-specific adaptation" (SSA), has been proposed as a possible single-neuron correlate of the mismatch negativity, a cortical evoked potential associated with stimulus novelty. Previous studies in cat did not observe SSA in single neurons in the auditory thalamus. However, these reports did not differentiate between the auditory thalamic subdivisions and did not examine the effects of changing the stimulus presentation rate. To explore the possibility of thalamic SSA more completely, we recorded extracellularly from 30 single units and 22 multiunit clusters in the ventral, medial, and dorsal subdivisions of the mouse medial geniculate body (MGB), while presenting the anesthetized animals with sequences of standard and deviant tones at interstimulus intervals of 400, 500 and 800 ms. We found SSA in the auditory thalamus at all three stimulus presentation rates, primarily in the medial subdivision but to a lesser degree also in the ventral MGB. Thalamic SSA was evident from the earliest onset of tone-evoked activity, although the latencies of responses to standard and deviant tones were not significantly different. Together with related findings of SSA in neurons of the "belt" regions of the inferior colliculus, these results demonstrate that SSA is present at subcortical levels, primarily in but not restricted to the nonlemniscal auditory pathway.

Figure 1.

Stimulus-specific adaptation in the mouse MGB. A, Population PSTHs averaged over all MGB recordings, showing responses to switching oddball stimuli with interstimulus intervals of 400 (left), 500 (middle), or 800 ms (right). Each plot compares the average neuronal response to tones presented as standards (blue) with the average response to the same tones presented as deviants (red); the average difference in response is also shown (green). B, Histograms of neuronal stimulus-specific adaptation indices (neuronal SIs) for tone responses recorded using switching-oddball stimuli with interstimulus intervals of 400 (left), 500 (middle), or 800 ms (right). Recordings with individually significant neuronal SIs (p < 0.01) are indicated with black bars. Numbers and text within each plot indicate the following: (bottom left and right) the number of recordings with neuronal SIs above and below zero; (top left) the result of a sign-rank test of the hypothesis that the median neuronal SI was zero; and (top right) the percentage of recordings for which the neuronal SI was individually significant by a randomization test (p < 0.01). C, Population PSTHs showing responses averaged over only those MGB recordings for which the neuronal SIs were significant (p < 0.01) and with an expanded timescale around response onset. Conventions as in A but note different x-scale and y-scale.

Figure 2.

Stimulus-specific adaptation occurs primarily in the medial subdivision of the mouse MGB. Plotting conventions as in Figure 1B. Histograms show neuronal SIs for recordings in the medial (A), ventral (B), and dorsal (C) MGB, for each of the three different interstimulus intervals.