Opiate receptor gradients in monkey cerebral cortex: correspondence with sensory processing hierarchies.

In order to obtain information on the possible functions of endogenous opiates in the primate cerebral cortex, we assessed the distribution of mu-like opiate receptors (which selectively bind 3H-labeled naloxone) and delta-like opiate receptors (which selectively bind 3H-labeled D-Ala2, D-Leu5-enkephalin) throughout the cerebral cortex of the rhesus monkey. Stereospecific [3H]naloxone binding sites increased in a gradient along hierarchically organized cortical systems that sequentially process modality-specific sensory information of a progressively more complex nature. Specific [3H]enkephalin binding sites, in contrast, were relatively evenly distributed throughout the cerebral cortex. These results, in combination with electrophysiological studies of monkeys and humans, suggest that mu-like opiate receptors may play a role in the affective filtering of sensory stimuli at the cortical level, that is, in emotion-induced selective attention.

[1]  P. Maclean.  CEREBRAL EVOLUTION AND EMOTIONAL PROCESSES: NEW FINDINGS ON THE STRIATAL COMPLEX , 1972, Annals of the New York Academy of Sciences.

[2]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[3]  H. E. Rosvold,et al.  Analysis of the delayed-alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkey. , 1971, Journal of comparative and physiological psychology.

[4]  John Hughes,et al.  Endogenous opioid peptides: multiple agonists and receptors , 1977, Nature.

[5]  J. M. Ree,et al.  ADRENOCORTICOTROPHIC HORMONE FRAGMENTS MIMIC THE EFFECT OF MORPHINE in vitro , 1978, British journal of pharmacology.

[6]  K. Pribram,et al.  Selective attention: input filter or response selection? An electrophysiological analysis. , 1972, Brain research.

[7]  Deepak N. Pandya,et al.  Further observations on corticofrontal connections in the rhesus monkey , 1976, Brain Research.

[8]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[9]  A Reeves,et al.  Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey. , 1971, Brain research.

[10]  A. Björklund,et al.  Regional distribution of catecholamines in monkey cerebral cortex, evidence for a dopaminergic innervation of the primate prefrontal cortex , 1978, Neuroscience Letters.

[11]  F. Bloom,et al.  Neuronal actions of endorphins and enkephalins among brain regions: a comparative microiontophoretic study. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[12]  F. Norris,et al.  Enkephalin-induced depression of single neurons in brain areas with opiate receptors--antagonism by naloxone. , 1976, Science.

[13]  M Mishkin,et al.  Organization of the amygdalopetal projections from modality‐specific cortical association areas in the monkey , 1980, The Journal of comparative neurology.

[14]  A. Goldstein.  Opioid peptides endorphins in pituitary and brain. , 1976, Science.

[15]  S. Snyder,et al.  Opiate receptor binding in rhesus monkey brain: association with limbic structures , 1978, Brain Research.

[16]  C. Rosenkilde,et al.  Functional heterogeneity of the prefrontal cortex in the monkey: a review. , 1979, Behavioral and neural biology.

[17]  D. Pandya,et al.  Interhemispheric projections of the parietal lobe in the rhesus monkey. , 1969, Brain research.

[18]  S. Snyder,et al.  Regional Distribution of Opiate Receptor Binding in Monkey and Human Brain , 1973, Nature.

[19]  S. Snyder,et al.  The regional distribution of a morphine-like factor enkephalin in monkey brain , 1976, Brain Research.

[20]  K. Pribram,et al.  Neuronographic analysis of medial and basal cerebral cortex. II. Monkey. , 1953, Journal of neurophysiology.

[21]  W. Fries,et al.  Opiate agonist-antagonist interaction at cortical neurones of naive and tolerant/dependent rats. , 1974, Brain research.

[22]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[23]  Mortimer Mishkin,et al.  Analogous neural models for tactual and visual learning , 1979, Neuropsychologia.

[24]  G. V. Hoesen,et al.  Temporal neocortical afferent connections to the amygdala in the rhesus monkey , 1976, Brain Research.

[25]  W. Nauta,et al.  Fibre degeneration following lesions of the amygdaloid complex in the monkey. , 1961, Journal of anatomy.

[26]  M. Mishkin,et al.  Emotional Responses Toward Humans in Monkeys with Selective Frontal Lesions , 1968 .

[27]  A. Crane,et al.  Regional distribution of monoamines in the cerebral cortex and subcortical structures of the rhesus monkey: concentrations and in vivo synthesis rates , 1979, Brain Research.

[28]  H. Y. Yang,et al.  Regional distribution of leu and met enkephalin in rat brain , 1977, Neuropharmacology.

[29]  M. Palkovits,et al.  Norepinephrine and dopamine in the limbic system of the rat. , 1974, Brain research.

[30]  L. H. Miller,et al.  Polypeptide influences on attention, memory and anxiety in man. , 1974, Pharmacology, biochemistry, and behavior.

[31]  L. Stein,et al.  Enkephalin may mediate euphoria and drive-reduction reward , 1977, Nature.

[32]  R. Hill,et al.  Depression of nociceptive and other neurones in the brain by iontophoretically applied met-enkephalin , 1976, Nature.

[33]  F. Bloom,et al.  Regional dissociation of beta-endorphin and enkephalin contents in rat brain and pituitary. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[34]  W. Nauta,et al.  Subcortical projections from the temporal neocortex in Macaca mulatta , 1956 .

[35]  W. Nauta,et al.  Neural associations of the amygdaloid complex in the monkey. , 1962, Brain : a journal of neurology.

[36]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[37]  J. Stewart,et al.  Electrophysiological effects of enkephalin analogs in rat cortex. , 1978, Life sciences.

[38]  R. E. Passingham,et al.  Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta) , 1980, Brain Research.

[39]  T. Biscoe,et al.  Effect of etorphine, morphine and diprenorphine on neurones of the cerebral cortex and spinal cord of the rat , 1972, British journal of pharmacology.

[40]  Role of the inferotemporal cortex in visual selective attention. , 1979, Electroencephalography and clinical neurophysiology.

[41]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[42]  M. Herkenham,et al.  In vitro autoradiography of opiate receptors in rat brain suggests loci of "opiatergic" pathways. , 1980, Proceedings of the National Academy of Sciences of the United States of America.