Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity

The 2-deoxyglucose (2-DG) method was used to map the metabolic activity of the auditory cortex (AC) during and after conditioning. Using separate groups of animals, the effects of both paired and unpaired presentations of a 4-5 kHz FM tone (CS) and midbrain reticular stimulation (US) were compared for acquisition, extinction and sensitization training. Rats with cardiac deceleration conditioned to the FM tone showed a pattern of AC metabolic activity distinctly different from that seen in control animals. The tonotopic pattern of 2-DG labeling consisted of two contiguous spindle-shaped bands corresponding to the location of neurons with best frequency response in the 4-5 kHz band width. Reticular stimulation alone or combined with the tones produced a widespread increase of 2-DG uptake. At least two types of modulatory effects appeared to interact with the tonotopic pattern. The first involved a selective enhancement of evoked activity in the AC region of convergence of CS-US effects. This effect may be related to learning because it was restricted to the conditioning group. The second effect involved a general increase in background uptake of 2-DG in AC. This effect may be related to reticular sensitization because it was common to all groups subjected to reticular stimulation. The present findings are the first anatomical demonstration of the modulatory effects of auditory learning on AC metabolic activity.

[1]  B. Hart Experimental Neuropsychology: a Laboratory Manual; , 1969 .

[2]  Henning Scheich,et al.  Classical conditioning of tone-signaled bradycardia modifies 2-deoxyglucose uptake patterns in cortex, thalamus, habenula, caudate-putamen and hippocampal formation , 1986, Brain Research.

[3]  F. Gonzalez-Lima,et al.  Classical conditioning enhances auditory 2-deoxyglucose patterns in the inferior colliculus , 1984, Neuroscience Letters.

[4]  Henning Scheich,et al.  Ascending reticular activating system in the rat: A 2-deoxyglucose study , 1985, Brain Research.

[5]  A Sakaguchi,et al.  Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  A. Ryan,et al.  Behavioral Modification of Response Characteristics of Cells in the Auditory System , 1982 .

[7]  D. Diamond,et al.  Initial events in conditioning: Plasticity in the pupillomotor and auditory systems , 1984 .

[8]  J. H. Chin,et al.  FACTORS AFFECTING SENSORY INPUT IN THE CAT: MODIFICATON OF EVOKED AUDITORY POTENTIALS BY RETICULAR FORMATION. , 1965, Electroencephalography and clinical neurophysiology.

[9]  D H HUBEL,et al.  "Attention" Units in the Auditory Cortex , 1959, Science.

[10]  R. Mark,et al.  Fear and the modification of acoustically evoked potentials during conditioning. , 1967, Journal of neurophysiology.

[11]  J. Disterhoft,et al.  Trial sequence of changed unit activity in auditory system of alert rat during conditioned response acquisition and extinction. , 1976, Journal of neurophysiology.

[12]  D. Diamond,et al.  Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: I. Primary field (AI). , 1984, Behavioral neuroscience.

[13]  M. H. Goldstein,et al.  Evoked unit activity in auditory cortex of monkeys performing a selective attention task , 1976, Brain Research.

[14]  Henning Scheich,et al.  Functional activation in the auditory system of the rat produced by arousing reticular stimulation: a 2-deoxyglucose study , 1984, Brain Research.

[15]  M. Reivich,et al.  Functional neuroanatomy of the auditory cortex studied with [2-14C]deoxyglucose , 1981, Experimental Neurology.

[16]  J. Kelly Polysensory cortical lesions and auditory temporal pattern discriminations in the cat. , 1974, Brain research.

[17]  A. W. Bell Enchytraeus fragmentosus, a New Species of Naturally Fragmenting Oligochaete Worm , 1959, Science.

[18]  K. Casey,et al.  Rewarding and aversive brain stimulation opposite effects on medial thalamic units. , 1973, Physiology & behavior.

[19]  W. Oldendorf,et al.  Kinetics of Transport and Phosphorylation of 2‐Fluoro‐2‐Deoxy‐d‐Glucose in Rat Brain , 1983, Journal of neurochemistry.

[20]  J S Buchwald,et al.  Classical conditioning with auditory discrimination of the eye blink in decerebrate cats. , 1977, Science.

[21]  W. Wickelgren Effect of state of arousal on click-evoked responses in cats. , 1968, Journal of neurophysiology.

[22]  Shigenori Watanabe,et al.  Potentiation of pressor and behavioral responses to brain stimulation following bilateral olfactory bulbectomy in freely moving rats , 1980, Brain Research Bulletin.

[23]  J. Popelář,et al.  Functional Organization of the Inferior Colliculus , 1981 .

[24]  B. Bohus,et al.  Attenuation by arginine- and desglycinamide-lysine-vasopressin of a centrally evoked pressor response. , 1982, Journal of the autonomic nervous system.

[25]  R. Hienz,et al.  Electrophysiologic studies of the auditory cortex in the awake monkey. , 1980, American journal of otolaryngology.

[26]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[27]  Henning Scheich,et al.  Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. I. Activation of auditory nuclei , 1984, Behavioural Brain Research.

[28]  JOHN W. Moore,et al.  Conditioned inhibition of the nictitating membrane response in decorticate rabbits , 1980, Behavioural Brain Research.