Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. I. Activation of auditory nuclei

The 2-deoxyglucose (2-DG) autoradiographic method was used to map the metabolic activity of auditory nuclei before, during and after conditioning. The experiment involved freely behaving rats in a Pavlovian conditioning paradigm in which a 4-5 kHz frequency modulated tone (CS) was paired with aversive electrical stimulation of the midbrain reticular formation (US). The unconditioned response was a rapid decrease in heart rate evoked by the US. Eight groups of rats were subjected to: (1) the tone CS before conditioning; (2) the US alone; (3) the paired CS-US (acquisition); (4) the tone CS after conditioning (extinction); (5) the US prior to the CS (sensitization); (6) the unpaired CS-US (pseudoconditioning); (7) the CS after pseudoconditioning; and (8) no stimulation. The major finding was the differential effect produced by the same tone before and after conditioning. The results showed that: (a) reticular mechanisms interact with incoming acoustic stimuli and modulate the response of auditory nuclei; (b) within each auditory nucleus the region of overlap of the spatial representations of CS and US developed an enhanced metabolic response during conditioning; and (c) the CS representation within the neuronal space of the tonotopic maps in all auditory nuclei, with the exception of the medial geniculate, reflected the learned behavioral value of the CS. The changes revealed by the 2-DG method represent the first anatomical demonstration of the activating effects of reticular sensitization and conditioning on a sensory system. The observations support the conclusion that auditory responses are dependent on the physical as well as on the behavioral parameters of a stimulus.

[1]  C. Woody Conditioning : representation of involved neural functions , 1982 .

[2]  G. A. Clark,et al.  Activity of Dentate Gyrus During NM Conditioning in Rabbit , 1982 .

[3]  Eric R. Kandel,et al.  Classical Conditioning in Aplysia: Neuronal Circuits Involved in Associative Learning , 1982 .

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

[5]  K. Takamatsu,et al.  Metabolic mapping of chick brain after imprinting using [14C]2-deoxyglucose technique , 1979, Brain Research.

[6]  Regional brain uptake of 2-deoxy-D-glucose following training in a discriminated y-maze avoidance task. , 1982, Journal of comparative and physiological psychology.

[7]  W. R. Webster,et al.  Autroradiographic demonstration with 2-[14C]deoxyglucose of frequency selectivity in the auditory system of cats under conditions of functional activity , 1978, Neuroscience Letters.

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

[9]  A. L. Beggs,et al.  Associative Processes in Spinal Reflexes , 1982 .

[10]  James L Olds,et al.  Patterns of conditioned unit responses in the auditory system of the rat , 1978, Experimental Neurology.

[11]  A. Ryan,et al.  Effects of behavioral performance on single-unit firing patterns in inferior colliculus of the rhesus monkey. , 1977, Journal of neurophysiology.

[12]  Masao Ito Synaptic Plasticity Underlying the Cerebellar Motor Learning Investigated in Rabbit’s Flocculus , 1982 .

[13]  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.

[14]  D. Birt,et al.  Separation of associative from non-associative short latency changes in medial geniculate and inferior colliculus during differential conditioning and reversal in rats , 1979, Brain Research.

[15]  F. Sharp,et al.  Increasing intensities of wide band noise increase [14C]2-deoxyglucose uptake in gerbil central auditory structures , 1981, Brain Research.

[16]  James Olds,et al.  Midbrain unit activity during classical conditioning , 1977, Brain Research.

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

[18]  R. Hernández-Peón,et al.  Modification of electric activity in cochlear nucleus during attention in unanesthetized cats. , 1956, Science.

[19]  Josef M. Miller,et al.  Single cell activity in the auditory cortex of the unanesthetized, behaving monkey: Correlation with stimulus controlled behavior , 1975, Brain Research.

[20]  D. Birt,et al.  Associative response changes in lateral midbrain tegmentum and medial geniculate during differential appetitive conditioning. , 1981, Journal of neurophysiology.

[21]  F. Sharp,et al.  Tonotopic organization in the central auditory pathway of the mongolian gerbil: A 2‐deoxyglucose study , 1982, The Journal of comparative neurology.

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

[23]  H. Scheich,et al.  Acoustic imprinting leads to differential 2-deoxy-D-glucose uptake in the chick forebrain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[24]  M. Gabriel,et al.  Mechanism and Generality of Stimulus Significance Coding in a Mammalian Model System , 1982 .

[25]  J. Buchwald,et al.  Changes in cortical and subcortical unit activity during behavioral conditioning , 1966 .

[26]  Herbert Voigt,et al.  The Internal Organization of the Dorsal Cochlear Nucleus , 1981 .

[27]  K. J. Klose,et al.  Functional metabolic mapping of a conditioned motor task in primates utilizing 2-[14C]deoxyglucose , 1981, Experimental Neurology.

[28]  J. Mcculloch,et al.  A potential error in modifications of the [14C]2-deoxyglucose technique , 1983, Brain Research.

[29]  Norman M. Weinberger,et al.  Effects of Conditioned Arousal on the Auditory System , 1982 .

[30]  Theodore W. Berger,et al.  Neuronal Substrates of learning and Memory: Hippocampus and Other Structures , 1982 .

[31]  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.

[32]  M. Gabriel,et al.  Multiple-unit activity of the rabbit medial geniculate nucleus in conditioning, extinction, and reversal , 1976 .

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

[34]  N. Weinberger,et al.  Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. , 1978, Behavioral biology.

[35]  J F Disterhoft,et al.  Learning centers of rat brain mapped by measuring latencies of conditioned unit responses. , 1972, Journal of neurophysiology.

[36]  D Sutton,et al.  Single Cell Activity in the Auditory Cortex of Rhesus Monkeys: Behavioral Dependency , 1972, Science.

[37]  N. Weinberger 16 – Neurophysiological Studies of Learning in Association with the Pupillary Dilation Conditioned Reflex1 , 1980 .

[38]  J. Fuster Cortical Neuron Activity in the Temporal Organization of Behavior , 1982 .

[39]  Norman M. Weinberger,et al.  Sensory Plasticity and Learning: The Magnocellular Medial Geniculate Nucleus of the Auditory System , 1982 .

[40]  F. Scalia The termination of retinal axons in the pretectal region of mammals , 1972, The Journal of comparative neurology.

[41]  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.

[42]  F. Sharp,et al.  Cochlear and middle ear effects on metabolism in the central auditory pathway during silence: A 2-deoxyglucose study , 1983, Brain Research.

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

[44]  Kandel Er Cellular insights into behavior and learning. , 1979 .

[45]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[46]  D. Cohen Central Processing Time for a Conditioned Response in a Vertebrate Model System , 1982 .

[47]  N. Weinberger,et al.  Modification of auditory and somatosensory system activity during pupillary conditioning in the paralyzed cat. , 1975, Journal of neurophysiology.

[48]  Walle J. H. Nauta,et al.  Some ascending pathways in the brain stem reticular formation. , 1958 .

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

[50]  D. Birt,et al.  Auditory Response Enhancement During Differential Conditioning in Behaving Rats , 1982 .

[51]  N. Tsukahara,et al.  Classical conditioning mediated by the red nucleus in the cat. , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  W. J. Mundl,et al.  Cardiovascular and respiratory responses to electrical stimulation of the midbrain in the rat. , 1983, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[53]  M. Gallagher,et al.  The Amygdala Central Nucleus: Contributions to Conditioned Cardiovascular Responding during Aversive Pavlovian Conditioning in the Rabbit , 1982 .