Stimulus-Specific Adaptation and Deviance Detection in the Rat Auditory Cortex

Abstract

Stimulus-specific adaptation (SSA) is the specific decrease in the response to a frequent (‘standard’) stimulus, which does not generalize, or generalizes only partially, to another, rare stimulus (‘deviant’). Stimulus-specific adaptation could result simply from the depression of the responses to the standard. Alternatively, there may be an increase in the responses to the deviant stimulus due to the violation of expectations set by the standard, indicating the presence of true deviance detection. We studied SSA in the auditory cortex of halothane-anesthetized rats, recording local field potentials and multi-unit activity. We tested the responses to pure tones of one frequency when embedded in sequences that differed from each other in the frequency and probability of the tones composing them. The responses to tones of the same frequency were larger when deviant than when standard, even with inter-stimulus time intervals of almost 2 seconds. Thus, SSA is present and strong in rat auditory cortex. SSA was present even when the frequency difference between deviants and standards was as small as 10%, substantially smaller than the typical width of cortical tuning curves, revealing hyper-resolution in frequency. Strong responses were evoked also by a rare tone presented by itself, and by rare tones presented as part of a sequence of many widely spaced frequencies. On the other hand, when presented within a sequence of narrowly spaced frequencies, the responses to a tone, even when rare, were smaller. A model of SSA that included only adaptation of the responses in narrow frequency channels predicted responses to the deviants that were substantially smaller than the observed ones. Thus, the response to a deviant is at least partially due to the change it represents relative to the regularity set by the standard tone, indicating the presence of true deviance detection in rat auditory cortex.

Auditory cortical and hippocampal local-field potentials to frequency deviant tones in urethane-anesthetized rats: An unexpected role of the sound frequencies themselves

“…If replicable, this finding also suggests a dissociation of non-contextual auditory processing (not sensitive to stimulus occurring probability) from contextual auditory processing (sensitive to stimulus occurring probability, Jääskeläinen et al, 2004;von der Behrens et al, 2009;May and Tiitinen, 2009;Taaseh et al, 2011) and further from auditory change detection per se (Näätänen, 1990;Farley et al, 2010). Such non-contextual mechanisms might play a key role to allow the attentional tuning of the auditory cortex to specific frequency content (da Costa et al, 2013) free from degradation by the repetition of a sound carrying this content.…”

“…Furthermore, similarly to MMN (Jacobsen and Schröger, 2001), differential brain responses in animals have been attributed to deviant tones as changes in the repetitiveness of a standard tone rather than as rare tones relative to the standard tone (e.g., Ruusuvirta et al, 1998;Nakamura et al, 2011;Taaseh et al, 2011;Jung et al, 2013;Shiramatsu et al, 2013;Harms et al, 2014;Malmierca et al, 2014). Together, these findings suggest that the mechanisms for automatic auditory change detection are not limited to the human brain.…”

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…Rare stimuli are not always salient. For example, a stimulus can appear in a sequence of multiple different stimuli, each being rarely presented but none is salient from the others (Taaseh et al 2011). The standard oddball paradigm cannot distinguish between the two possibilities.…”

“…The standard oddball paradigm cannot distinguish between the two possibilities. Despite recent attempts to resolve this issue for SSA in the auditory cortex, it still remains an open question (Furukawa et al 2005;Taaseh et al 2011). …”

“…Interestingly, no such facilitation was observed when the ISIs were smaller than 2 sec. In the short ISIs, the responses to the deviant stimulus were usually smaller than the responses to the same stimulus when presented alone (Reches and Gutfreund 2008a;Taaseh et al 2011). The facilitation of the responses to deviant stimuli occurred at late stages of the response, 150-200 ms after the onset of the stimulus.…”