Neural Responses in the Primary Auditory Cortex of Freely Behaving Cats While Discriminating Fast and Slow Click-Trains

Abstract

Repeated acoustic events are ubiquitous temporal features of natural sounds. To reveal the neural representation of the sound repetition rate, a number of electrophysiological studies have been conducted on various mammals and it has been proposed that both the spike-time and firing rate of primary auditory cortex (A1) neurons encode the repetition rate. However, previous studies rarely examined how the experimental animals perceive the difference in the sound repetition rate, and a caveat to these experiments is that they compared physiological data obtained from animals with psychophysical data obtained from humans. In this study, for the first time, we directly investigated acoustic perception and the underlying neural mechanisms in the same experimental animal by examining spike activities in the A1 of free-moving cats while performing a Go/No-go task to discriminate the click-trains at different repetition rates (12.5–200 Hz). As reported by previous studies on passively listening animals, A1 neurons showed both synchronized and non-synchronized responses to the click-trains. We further found that the neural performance estimated from the precise temporal information of synchronized units was good enough to distinguish all 16.7–200 Hz from the 12.5 Hz repetition rate; however, the cats showed declining behavioral performance with the decrease of the target repetition rate, indicating an increase of difficulty in discriminating two slower click-trains. Such behavioral performance was well explained by the firing rate of some synchronized and non-synchronized units. Trial-by-trial analysis indicated that A1 activity was not affected by the cat's judgment of behavioral response. Our results suggest that the main function of A1 is to effectively represent temporal signals using both spike timing and firing rate, while the cats may read out the rate-coding information to perform the task in this experiment.

Rapid Spectrotemporal Plasticity in Primary Auditory Cortex during Behavior

“…However, the sign of the plasticity change (i.e., which of the two stimuli is enhanced or suppressed) is influenced by other non-stimulus-related factors, such as task reward valence. Based on previous findings (Fritz et al, 2005a;David et al, 2012), we predicted that ⌬STRFs reflected enhanced responses to aversive stimuli (that the animal seeks to avoid) and suppressed responses to appetitive stimuli (that the animal seeks to approach).…”

“…This task-related optimization is influenced by context and task properties (task design, reward valence), by animal training history and motivation, and by the specific sensory stimuli involved (Beitel et al, 2003;Fritz et al, , 2005aFritz et al, , b, 2007Fritz et al, , 2010Brown et al, 2004;Blake et al, 2006;Polley et al, 2006;Selezneva et al, 2006;David et al, 2012;Guo et al, 2013). Thus, when detecting a target tone against a noisy background, the sensitivity of the receptive fields in primary auditory cortex (A1) rapidly changes at the frequency of the target tone Atiani et al, 2009).…”

“…Thus, when detecting a target tone against a noisy background, the sensitivity of the receptive fields in primary auditory cortex (A1) rapidly changes at the frequency of the target tone Atiani et al, 2009). The valence of the change depends on the meaning of the tone; if the tone is an aversive stimulus (negative reward), the change is positive (receptive field is sensitized at the target tone frequency); if the tone is associated with a positive reward, the change is negative (receptive field is suppressed at the target tone frequency) (Fritz et al, 2005a;David et al, 2012). These receptive field changes are not observed in behaviorally naive control animals when presented with identical acoustic sequences.…”

“…Our studies of rapid spectrotemporal receptive field (STRF) plasticity during behavior have focused on the spectral dimension by using purely spectral stimuli consisting of pure tones or tone complexes (Fritz et al, , 2005b. These studies have shown that the pattern of receptive field changes matches closely the spectral composition of the stimuli, a principle that we have referred to as the "matched-filter" hypothesis Atiani et al, 2009;Mesgarani et al, 2009;David et al, 2012).…”

“…These studies have shown that the pattern of receptive field changes matches closely the spectral composition of the stimuli, a principle that we have referred to as the "matched-filter" hypothesis Atiani et al, 2009;Mesgarani et al, 2009;David et al, 2012). Rapid adaptive changes, have also been observed along the temporal dimension when the tasks depended purely on the temporal parameters of the stimuli, such as when discriminating a change in click rates, the duration of a tone, and the amplitude modulations (Bao et al, 2004;Fritz et al, 2005b;Wassenhove and Nagarajan, 2007;Dong et al, 2011;Niwa et al, 2012;Shetake et al, 2012).…”