Research on auditory cortex plasticity.
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Biomedical subjects
Publications and source records attributed to J S Bakin.
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Auditory cortical receptive field plasticity produced during behavioral learning may be considered to constitute "physiological memory" because it has major characteristics of behavioral memory: associativity, specificity, rapid acquisition, and long-term retention. To investigate basal forebrain mechanisms in receptive field plasticity, we paired a tone with stimulation of the nucleus basalis, the main subcortical source of cortical acetylcholine, in the adult guinea pig. Nucleus basalis stimulation produced electroencephalogram desynchronization that was blocked by systemic and cortical atropine. Paired tone/nucleus basalis stimulation, but not unpaired stimulation, induced receptive field plasticity similar to that produced by behavioral learning. Thus paired activation of the nucleus basalis is sufficient to induce receptive field plasticity, possibly via cholinergic actions in the cortex.
Classical tone conditioning shifts frequency tuning in the auditory cortex to favor processing of the conditioned stimulus (CS) frequency versus other frequencies. This receptive field (RF) plasticity is associative, highly specific, rapidly acquired, and indefinitely retained-all important characteristics of memory. The investigators determined whether RF plasticity also develops during instrumental learning. RFs were obtained before and up to 24 hr after 1 session of successful 1-tone avoidance conditioning in guinea pigs. Long-term RF plasticity developed in all subjects (N = 6). Two-tone discrimination training also produced RF plasticity, like classical conditioning. Because avoidance responses prevent full elicitation of fear by the CS, long-term RF plasticity does not require the continual evocation of fear, suggesting that neural substrates of fear expression are not essential to RF plasticity.
Sensitization training with an auditory stimulus produces a general increase in response magnitude across the entire receptive field (RF) of neurons in the primary auditory cortex of the guinea pig (Bakin, J.S. and Weinberger, N.M., Brain Res., 536 (1990) 271-286). To determine if this effect reflects an auditory system-specific process or is caused by a process independent of the training stimulus modality, RFs in primary auditory cortex were characterized before and immediately after adult guinea pigs were given sensitization training with either an auditory or a visual training stimulus. General increases in auditory response magnitude across the RF were observed in 7 out of 7 auditory sensitization cases and 4 out of 5 visual sensitization cases. There were no statistical differences between the effects of auditory and visual sensitization training. These findings indicate that the general increases observed following sensitization training are the result of processes independent of CS modality, in contrast to the highly specific RF modifications that are caused by classical conditioning. The findings suggest that the 2 forms of RF plasticity, CS-specific re-tuning due to associative conditioning and polymodal general increases in gain due to non-associative sensitization, may reflect neural mechanisms involved in selective attention and vigilance, respectively.
To determine if classical conditioning produces general or specific modification of responses to acoustic conditioned stimuli (CS), frequency receptive fields (RF) of neurons in guinea pig auditory cortex were determined before and up to 24 h after fear conditioning. Highly specific RF plasticity characterized by maximal increased responses to the CS frequency and decreased responses to the pretraining best frequency (BF) and other frequencies was observed in 70% of conditioning cases. These opposing changes were often sufficient to produce a shift in tuning such that the frequency of the CS became the new BF. CS frequency specific plasticity was maintained as long as 24 h. Sensitization training produced general increased responses across the RF without CS specificity. The findings indicate that associative processes produce systematic modification of the auditory system's processing of frequency information and exemplify the advantages of combining receptive field analysis with behavioral training in the study of the neural bases of learning and memory.
The suprathreshold tonotopic organization of rat and guinea pig auditory cortex was investigated using intrinsic signal optical imaging through a thinned skull. Optical imaging revealed that suprathreshold pure sine wave tone stimulation (25-80 dB) evoked activity over large cortical areas that were tonotopically organized. Three-dimensional surface plots of the activated areas revealed "patchy' auditory-evoked activity consisting of numerous local peaks and valleys building to a maximum. Subsequent detailed electrophysiological mapping in the same subjects confirmed the localization of auditory-evoked activity based on optical imaging, including responses to a test frequency at cortical loci more than 2 octaves away from the threshold-defined isofrequency contour. The success of this technique in visualizing auditory cortex functional organization at suprathreshold stimulus levels will allow for future investigations of auditory cortex frequency representation, including representational plasticity induced by a variety of experimental manipulations.
It is well established that the functional organization of adult sensory cortices, including the auditory cortex, can be modified by deafferentation, sensory deprivation, or selective sensory stimulation. This paper reviews evidence establishing that the adult primary auditory cortex develops physiological plasticity during learning. Determination of frequency receptive fields before and at various times following aversive classical conditioning and instrumental avoidance learning in the guinea pig reveals increased neuronal responses to the pure tone frequency used as a conditioned stimulus (CS). In contrast, responses to the pretraining best frequency and other non-CS frequencies are decreased. These opposite changes are often sufficient to shift cellular tuning toward or even to the frequency of the CS. Learning-induced receptive field (RF) plasticity (i) is associative (requires pairing tone and shock), (ii) highly specific to the CS frequency (e.g., limited to this frequency +/- a small fraction of an octave), (iii) discriminative (specific increased response to a reinforced CS+ frequency but decreased response to a nonreinforced CS- frequency), (iv) develops extremely rapidly (within 5 trials, the fewest trials tested), and (v) is retained indefinitely (tested to 8 weeks). Moreover, RF plasticity is robust and not due to arousal, but can be expressed in the deeply anesthetized subject. Because learning- induced RF plasticity has the major characteristics of associative memory, it is therefore referred to as "physiological memory". We developed a model of RF plasticity based on convergence in the auditory cortex of nucleus basalis cholinergic effects acting at muscarinic receptors, with lemniscal and nonlemniscal frequency information from the ventral and magnocellular divisions of the medial geniculate nucleus, respectively. In the model, the specificity of RF plasticity is dependent on Hebbian rules of covariance. This aspect was confirmed in vivo using microstimulation techniques. Further, the model predicts that pairing a tone with activation of the nucleus basalis is sufficient to induce RF plasticity similar to that obtained in behavioral learning. This prediction has been confirmed. Additional tests of the model are described. RF plasticity is thought to translate the acquired significance of sound into an increased frequency representation of behaviorally important stimuli.