Stimulus-Specific Adaptation: Can It Be a Neural Correlate of Behavioral Habituation?

Abstract

Habituation is the most basic form of learning, yet many gaps remain in our understanding of its underlying neural mechanisms. We demonstrate that in the owl's optic tectum (OT), a single, low-level, relatively short auditory stimulus is sufficient to induce a significant reduction in the neural response to a stimulus presented up to 60 s later. This type of neural adaptation was absent in neurons from the central nucleus of the inferior colliculus and from the auditory thalamus; however, it was apparent in the OT and the forebrain entopallium. By presenting sequences that alternate between two different auditory stimuli, we show that this long-lasting adaptation is stimulus specific. The response to an odd stimulus in the sequence was not smaller than the response to the same stimulus when it was first in the sequence. Finally, we measured the habituation of reflexive eye movements and show that the behavioral habituation is correlated with the neural adaptation. The finding of a long-lasting specific adaptation in areas related to the gaze control system and not elsewhere suggests its involvement in habituation processes and opens new directions for research on mechanisms of habituation.

Large-Scale Synchronized Activity during Vocal Deviance Detection in the Zebra Finch Auditory Forebrain

“…This phenomenon is relatively long-lasting (up to 60 s) and operates both on artificial and natural stimuli (Netser et al, 2011). Its relationship with the type of sensitivity found in the present study remains as yet unclear because of differing stimulation paradigms; it may be that they represent two different mechanisms, but it may also be that secondary auditory forebrain circuits compute novelty of sound objects in natural auditory scenes and modulate tectal responses (Netser et al, 2011).…”

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

“…This was done in the OT of barn owls by presenting sequences of identical sounds and measuring unit responses as a function of the position of the stimulus in the sequence. Remarkably, it was found that the memory trace of the SSA in the OT can be up to 60 s long (Netser et al 2011). A single, short (300 ms), and low intensity (20 dB above threshold) stimulus was sufficient to induce a reduction in the neural response to the same stimulus occurring 60 s later.…”

“…Recently, auditory adaptation was characterized systematically in the barn owl's OT (Reches and Gutfreund 2008;Netser et al 2011). Oddball and repeated sequence protocols (see Fig.…”

“…Behavioral habituation does not comply with the above-mentioned principle of comparable time scales. For example, in the barn owl, reflexive pupil dilation and eye movements to sequences of relatively short stimuli with ISIs of 10-13 s readily habituated and recovered when the stimulus was switched from one type to another (Bala and Takahashi 2000;Spitzer et al 2003;Netser et al 2011).…”

“…One common model to explain SSA is that the two stimuli activate separate paths to the recorded neuron and that basic adaptation mechanisms (synaptic depression or intrinsic cellular mechanisms) act at levels where the activation is separated (Eytan et al 2003). An intriguing observation in the barn owl's SSA is a complete lack of cross-stimulus adaptation at long ISIs even though the frequency content of the two stimuli overlapped substantially (Netser et al 2011). It is therefore unlikely that this type of SSA is accounted for solely by basic response suppressions at lower, frequency-specific levels.…”