Conditioned tone control of brain reward behavior produces highly specific representational gain in the primary auditory cortex

Abstract

Primary sensory cortices have been assumed to serve as stimulus analyzers while cognitive functions such as learning and memory have been allocated to “higher” cortical areas. However, the primary auditory cortex (A1) is now known to encode the acquired significance of sound as indicated by associatively-induced specific shifts of tuning to the frequencies of conditioned stimuli (CS) and gains in area of CS representations. Rewarding brain stimulation can be a very powerful motivator and brain reward systems have been implicated in addictive behavior. Therefore, it is possible that a cue for brain reward will gain cortical territory and perhaps thereby increase its control of subsequent behavior. To investigate the effect of brain reward on cortical organization, adult male rats (n = 11) were first tested with varying amounts of stimulation of the ventral tegmental area (VTAstm) to generate sigmoidal psychometric functions of nose poke (NP) rates as a function of reward magnitude (duration). Next, we attempted to accomplish tone control of NPs by maintaining intertrial NPs using a low reward duration and presenting a 20 s tone (2.0 kHz, 70 dB) which signaled an increase in reward to a high magnitude 10 s after tone onset. Tone control was demonstrated by a significant increase in the rate of NPs during the first 10 s of tone presentation, which anticipated the delivery of the high magnitude of reward. Tone control was achieved in seven of 11 subjects. This was accompanied by a highly specific and significant gain in representational area, specifically for the half-octave range centered on the CS frequency. However, this plasticity developed only in tone-controlled (TC) animals. The auditory cortex of non-tone-controlled subjects (n = 4) did not differ from that of naïve controls (n = 9) although their VTAstm was as rewarding as for the TC group. These findings reveal that auditory instrumental behavior can be controlled by rewarding VTAstm and that such control appears necessary for the highly specific recruitment of cortical cells to increase the representation of a sound that acquires behavioral importance.

Sensory regulation of dopaminergic cell activity: Phenomenology, circuitry and function

“…Numerous studies have demonstrated that sensory processing in the cortex can be potentiated when associated with reward (e.g. Mogami and Tanaka, 2006;Hui et al, 2009;Franko et al, 2010;Hickey et al, 2010;Serences and Saproo, 2010;Weil et al, 2010). Our finding that the cortex can transmit information to DA neurons via the SC thus provides a mechanism by which short-latency sensory signals relayed to DA neurons can reflect stimulus value.…”

A Fully Automated and Highly Versatile System for Testing Multi-cognitive Functions and Recording Neuronal Activities in Rodents

“…Rewards: The final goal of the task is to obtain the reward ( Figure 5A-e and Figure 3). Behavioral tasks using this system can thus be easily designed to study many aspects of reward-decision issues and the function of the value systems of the brain [14][15][16][17] .…”

Optical imaging of plastic changes induced by fear conditioning in the auditory cortex

“…Insofar as such maps are comprised of the preferential tuning of neurons across these fields, and frequency tuning is shifted during learning, it might be expected that the signal frequency would develop an expanded representation in the map during auditory fear conditioning. Such frequency-specific increase in representational area has been found in instrumental reward tasks involving training over months or weeks (Recanzone et al 1993;Rutkowski and Weinberger 2005;Hui et al 2009;Bieszczad and Weinberger 2010a, b). However, still unknown is whether such map expansions can develop as rapidly as tuning shifts Weinberger 2004).…”