Neurons in auditory cortex are sensitive to the probability of stimuli: responses to rare stimuli tend to be stronger than responses to common ones. Here, intra- and extracellular recordings from the auditory cortex of halothane-anesthetized rats revealed the existence of a finer sensitivity to the structure of sound sequences. Using oddball sequences in which the order of stimulus presentations is periodic, we found that tones in periodic sequences evoked smaller responses than the same tones in random sequences. Significant reduction in the responses to the common tones in periodic relative to random sequences occurred even when these tones consisted of 95% of the stimuli in the sequence. The reduction in responses paralleled the complexity of the sound sequences and could not be explained by short-term effects of clusters of deviants on succeeding standards. We conclude that neurons in auditory cortex are sensitive to the detailed structure of sound sequences over timescales of minutes.
Stimulus-specific adaptation (SSA) is the reduction in response to a common stimulus that does not generalize, or only partially generalizes, to rare stimuli. SSA is strong and widespread in primary auditory cortex (A1) of rats, but is weak or absent in the main input station to A1, the ventral division of the medial geniculate body. To study SSA in A1, we recorded neural activity in A1 intracellularly using sharp electrodes. We studied the responses to tone pips of the same frequency in different contexts: as Standard and Deviants in Oddball sequences; in equiprobable sequences; in sequences consisting of rare tone presentations; and in sequences composed of many different frequencies, each of which was rare. SSA was found both in subthreshold membrane potential fluctuations and in spiking responses of A1 neurons. SSA for changes in frequency was large at a frequency difference of 44% between Standard and Deviant, and clearly present with tones separated by as little as 4%, near the behavioral frequency difference limen in rats. When using equivalent measures, SSA in spiking responses was generally larger than the SSA at the level of the membrane potential. This effect can be traced to the nonlinearity of the transformation between membrane potential to spikes. Using the responses to the same tone in different contexts made it possible to demonstrate that cortical SSA could not be fully explained by adaptation in narrow frequency channels, even at the level of the membrane potential. We conclude that local processing significantly contributes to the generation of cortical SSA.
Detecting rare and surprising events is a useful strategy for sensory -systems. In the human auditory system, deviance detection is indexed by an important component of the auditory event-related potentials, the mismatch negativity (MMN). Responses of single neurons in the inferior colliculus, medial geniculate body, and auditory cortex of mammals (cats, rats, and mice) show responses that share some properties with MMN: they are evoked by rare events, are preattentive (in as much as they occur in anesthetized animals), and, at least at the level of primary auditory cortex, cannot be accounted for by simple fatigue of the incoming sensory information. Here we extend these results to deviations beyond tone frequency. Recording in rat primary auditory cortex and using oddball sequences consisting of two frozen tokens of broadband noise samples, we found differences between the responses to the same token when used as the common and when used as the deviant, showing an exquisite sensitivity to the small differences between two spectro-temporally similar sounds. Similarly, differential adaptation can be demonstrated when using two word-like stimuli that have been derived from human speech but adapted to the rat auditory system. Thus, differential adaptation to common and rare sounds is present also with sounds whose complexity mirrors that of natural environments.
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