Modification of auditory and somatosensory system activity during pupillary conditioning in the paralyzed cat

Abstract

The role of sensory systems in the development of behavioral conditioned responses was investigated by recording multiple-unit activity in the auditory and somatosensory pathways during Pavlovian conditioning of the pupillary-dilation responses of paralyzed cats. Establishment of conditioned pupillary-dilation responses to a white noise CS+, pupillary discrimination between the CS+ and a tone CS-, and subsequent discrimination reversal provided the behavioral foundation for examining neural changes related to behavioral learning. Multiple-unit responses to the acoustic CS+ were significantly enhanced in the auditory cortex, cochlear nucleus, and somatic cortex, but not in the cuneate nucleus. The possibility that these effects could be due to changes in stimulus intensity at the sensory receptor, to mo-ement artifacts, or to feedback from skeletal responses were ruled out because the animals were immobilized. Nor could these neural changes be attributable to sensitization, as those brain areas which showed conditioned enhancement to the CS+ exhibited significantly larger responses to the CS+ than to the CS-. Furthermore, the changes in neural activity followed the significance of the CS; after reversal of the reinforcement contingencies, the amount of multiple-unit activity evoked by the stimuli gradually reversed too. Although the somatic cortex showed conditioning and discrimination, greater stimulus specificity was found in the auditory system. Only in the somatic cortex was there a significant increase in responses to the CS- as well as the CS4. Furthermore, both somatosensory loci exhibited enhanced responses to those tactile probes presented during the acoustic CS, suggesting a phasic increase in neural excitability to all stimuli. Analysis of the number of trials required to attain an acquisition criterion indicated that the neural changes occurred first in the auditory cortex, then the cochlear nucleus, followed in turn by the somatic cortex, and finally the cuneate nucleus. However, none of these neural changes preceded acquisition of conditioned pupillary dilations. These results suggest that sensory system changes are not essential for the initial associative process. These findings indicate that the study of autonomic conditioned responses may prove beneficial in seeking the critical neural events which underlie the initial association between two stimuli. A hypothetical model, which explains the development of pupillary and sensory system conditioned responses, was also presented.

Modulation of auditory cortex unit activity during the performance of a conditioned response

“…The behavioral paradigm was a modification of the pupillary conditioning task elaborated in the paralyzed cat by Weinberger et al (16,17). White noise was the conditioned stimulus, tail shock was the unconditioned stimulus, and the behavioral response was pupillary dilation.…”

“…They are dependent in part on nonacoustic variables such as the sleep-waking cycle (2, 3, 14, 18-ZO), experience (4,6,9,13,16), and anesthesia (7,8,10). Such nonsensory variables may be considered to determine the state of the animal.…”

Learning related activation of somatosensory cortex by an auditory stimulus recorded with magnetoencephalography

“…In a tone discrimination task in which auditory stimuli were preceded by the presentation of a light, activation was found in the auditory cortex following presentation of the light, prior to the onset of the auditory stimuli (Brosch et al, 2005). These conditioned neural responses were not significantly correlated with the acquisition and maintenance of conditioned autonomic responses, such as pupil dilation (Oleson et al, 1975). Thus, CRs can be measured from primary sensory regions, and these CRs behave analogously to those recorded from peripheral tissue.…”

“…For example, neurons in the primary auditory cortex responded to tactile stimulation alone prior to conditioning (Dumenko and Sachenko, 1981). Similarly, neurons in the primary somatosensory cortex responded to auditory stimuli alone prior to any training (Oleson et al, 1975). Thus, primary sensory cortical regions show the capacity to respond to cross-modal stimulation.…”

“…Further, following conditioning training using an auditory conditioned stimulus paired with a somatosensory (electrical stimulation) unconditioned stimulus, neurons in somatosensory ( [Dolbakyan, 1982] and [Oleson et al, 1975]) and motor cortices (Dolbakyan, 1982) showed enhanced responding to the auditory CS with similar firing patterns to those in the auditory cortex. Within a differential conditioning paradigm that incorporated one auditory stimulus that was paired with the somatosensory US (CS+), and one that was unpaired (CS−), neurons in the somatosensory cortex showed increased responses to both auditory stimuli, although the response to the CS+ became significantly greater than to the CS− (Oleson et al, 1975). In a tone discrimination task in which auditory stimuli were preceded by the presentation of a light, activation was found in the auditory cortex following presentation of the light, prior to the onset of the auditory stimuli (Brosch et al, 2005).…”