Abstract
Stimulus-specific adaptation (SSA) occurs when the spike rate of a neuron decreases with repetitions of the same stimulus, but recovers when a different stimulus is presented. It has been suggested that SSA in single auditory neurons may provide information to change detection mechanisms evident at other scales (e.g., mismatch negativity in the event related potential), and participate in the control of attention and the formation of auditory streams. This article presents a spiking-neuron model that accounts for SSA in terms of the convergence of depressing synapses that convey feature-specific inputs. The model is anatomically plausible, comprising just a few homogeneously connected populations, and does not require organised feature maps. The model is calibrated to match the SSA measured in the cortex of the awake rat, as reported in one study. The effect of frequency separation, deviant probability, repetition rate and duration upon SSA are investigated. With the same parameter set, the model generates responses consistent with a wide range of published data obtained in other auditory regions using other stimulus configurations, such as block, sequential and random stimuli. A new stimulus paradigm is introduced, which generalises the oddball concept to Markov chains, allowing the experimenter to vary the tone probabilities and the rate of switching independently. The model predicts greater SSA for higher rates of switching. Finally, the issue of whether rarity or novelty elicits SSA is addressed by comparing the responses of the model to deviants in the context of a sequence of a single standard or many standards. The results support the view that synaptic adaptation alone can explain almost all aspects of SSA reported to date, including its purported novelty component, and that non-trivial networks of depressing synapses can intensify this novelty response.
Highlights
Natural acoustic environments play host to a wide variety of sounds that are either repetitive or follow a regular pattern
This study offers three distinct contributions to the ongoing discussion concerning stimulus-specific adaptation in single neurons: a new model of Stimulus-specific adaptation (SSA) that accounts for an array of experimental results; a description of a novel stimulus paradigm, Author Summary
The average responses to deviants presented in the two contexts are compared to delineate the effect of the context on the processing of the same sound. (Note that in the many standards condition, the term ‘deviant’ is employed in a nominal sense, as it refers to the true deviant in the corresponding oddball sequence.) The signal is enhanced when the deviant tone is presented against a background of a single standard, and the same is true for the spiking responses of single cortical neurons [7], which we aim to model here
Summary
Natural acoustic environments play host to a wide variety of sounds that are either repetitive or follow a regular pattern. SSA in response to tone sequences has been measured in the spiking of single neurons at various stages of the auditory pathway, including the inferior colliculus (IC) in the rat [2,3], medial geniculate body (MGB) of the thalamus in the mouse [4] and rat [5], thalamic reticular nucleus in the rat [6], and primary auditory cortex in the cat [7,8] and rat [9] It has been suggested [7,8,10] that SSA in single neurons lies on the path leading to the generation of mismatch negativity (MMN)–a frontocentrally negativegoing deflection in the event-related potential [11,12], evoked in response to violations of an established temporal sound pattern, including changes in frequency, intensity, duration and even the omission of an expected stimulus (for a recent review, see [13]). It is thought that MMN, in turn, may be implicated in the redirection of attention [14], maintain the representation of the auditory context [12], and contribute to auditory scene analysis [12,15]
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