Searching for the Mismatch Negativity in Primary Auditory Cortex of the Awake Monkey: Deviance Detection or Stimulus Specific Adaptation?

Abstract

The mismatch negativity (MMN) is a pre-attentive component of the auditory event-related potential that is elicited by a change in a repetitive acoustic pattern. While MMN has been extensively utilized in human electrophysiological studies of auditory processing, the neural mechanisms and brain regions underlying its generation remain unclear. We investigate possible homologues of the MMN in macaque primary auditory cortex (A1) using a frequency oddball paradigm in which rare ‘deviant’ tones are randomly interspersed among frequent ‘standard’ tones. Standards and deviants had frequencies equal to the best frequency (BF) of the recorded neural population or to a frequency that evoked a response half the amplitude of the BF response. Early and later field potentials, current source density components, multiunit activity, and induced high gamma band responses were larger when elicited by deviants than by standards of the same frequency. Laminar analysis indicated that differences between deviant and standard responses were more prominent in later activity, thus suggesting cortical amplification of initial responses driven by thalamocortical inputs. However, unlike the human MMN, larger deviant responses were characterized by the enhancement of ‘obligatory’ responses rather than the introduction of new components. Furthermore, a control condition wherein deviants were interspersed among many tones of variable frequency replicated the larger responses to deviants under the oddball condition. Results suggest that differential responses under the oddball condition in macaque A1 reflect stimulus-specific adaptation rather than deviance detection per se. We conclude that neural mechanisms of deviance detection likely reside in cortical areas outside of A1.

Disruption of hierarchical predictive coding during sleep

“…Unlike predictive coding, adaptation is considered a basic property of bottom-up sensory transmission localized to the primary auditory cortex (23,28,56). We indeed showed that the early MMR effect localizes almost exclusively to auditory areas during both wakefulness and sleep (Fig.…”

Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

“…This result highlights a selective role of frontal structures in computing a PE. A featurebased adaptation mechanism, as seen in the auditory cortex (13,31,45), is expected to produce a response independent of the degree of periodicity of occurrence of deviants. Because on average, the probability of stimuli in the predictable and unpredictable sequences was identical, a purely adaptation-based model (31) would not predict the differential activity that we found in frontal electrodes.…”

“…This differentiation is critical, because the Hγ has distinct response properties compared with LF-ERPs (11). Using intracranial recordings, involvement of low frequency-evoked activity and Hγ-induced activity in auditory PE signals were found in temporal regions (12,13), where Hγ amplitude was shown to increase earlier than lower-frequency bands (12). In inferior frontal regions, previous ECoG studies (12,14) did not find evidence for Hγ frontal activity in response to local deviations [as opposed to global ones; discussed in the work by El-Karoui et al (14)], although low-frequency effects were reported in some (15,16) but not all (17) studies.…”

A roadmap for the study of conscious audition and its neural basis

“…While this is suggested by their latency and by the fact that similar negativities in monkeys arise from superficial cortical layers [272], more work is needed, particularly in establishing NCC A experiments in non-human primates.…”