Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum

The lateral amygdaloid nucleus (AL) is anatomically connected with sensory processing structures in the thalamus and cortex and is believed to be critically involved in emotional processing by virtue of these connections. In order to understand further how auditory projections to AL contribute to emotional processing, acoustic response properties of single AL neurons were characterized in rats. Recordings were also made in the posterior striatum dorsal to AL. Many cells in AL and the striatum could be driven by broad-band auditory stimulation with white noise or clicks. Initial onset latencies were typically between 12 and 25 msec. Most cells also had later responses (60–150 msec), and a few only had late responses. In frequency receptive field tests, different classes of cells were identified. One group had relatively clear frequency preferences. Thresholds for these relatively tuned cells tended to be somewhat higher in AL than in the striatum. Frequency preferences for AL cells were always above 10 kHz. Although most striatal cells had preferences for frequencies above 10 kHz, some cells were found with frequencies below 10 kHz as well. A second group of acoustically responsive neurons, much more common in AL than in the striatum, showed no frequency specificity (untuned cells). These responded to a wide range of frequencies, even at intensities near threshold. A third group, found mainly in AL (approximately 60% of the total population of cells examined in AL), exhibited rapid habituation to auditory stimuli. These tended to have high thresholds (80–100 dB). Because these cells habituated so quickly, frequency specificity could not be determined. Responses in AL and the striatum were compared with responses in the “specific” auditory relay nucleus of the thalamus, the ventral division of the medial geniculate body, where cells had shorter onset latencies, narrower tuning functions, and lower-intensity thresholds than cells in AL and striatal areas. These findings show that cells in AL exhibit a wide range of auditory tuning properties and suggest that information processing in the amygdala might be fruitfully studied as a direct extension of processing in sensory afferent structures.

[1]  Alex Wilson,et al.  A neuro - anatomical systems analysis of conditioned bradycardia in the rabbit , 1991 .

[2]  F. T. Russchen,et al.  Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques , 1982, The Journal of comparative neurology.

[3]  Joseph E LeDoux,et al.  Unit responses evoked in the amygdala and striatum by electrical stimulation of the medial geniculate body , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[5]  E. Yeterian,et al.  Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections , 1978, Brain Research.

[6]  J. Newman,et al.  Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. , 1973, Brain research.

[7]  E. Rolls A Theory of Emotion, and its Application to Understanding the Neural Basis of Emotion , 1990 .

[8]  Joseph E LeDoux,et al.  Topographic organization of neurons in the acoustic thalamus that project to the amygdala , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  A. McDonald,et al.  Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat , 1984, The Journal of comparative neurology.

[10]  E. Rolls,et al.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey , 1979, Experimental Neurology.

[11]  J. Buchwald,et al.  Acoustic responses and plasticity of limbic units in cats. , 1973, Experimental neurology.

[12]  W Rhode,et al.  Auditory physiology. , 1982, Science.

[13]  The Psycho- and Neurobiology of Fear Systems in the Brain , 1991 .

[14]  J. Fuster,et al.  Reactivity of limbic neurons of the monkey to appetitive and aversive signals. , 1971, Electroencephalography and clinical neurophysiology.

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

[16]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

[17]  L. Brothers,et al.  Response of neurons in the macaque amygdala to complex social stimuli , 1990, Behavioural Brain Research.

[18]  J. Veening Subcortical afferents of the amygdaloid complex in the rat: an HRP study , 1978, Neuroscience Letters.

[19]  O D Creutzfeldt,et al.  Anatomy of the auditory thalamocortical system of the guinea pig , 1989, The Journal of comparative neurology.

[20]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

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

[22]  J. Winer,et al.  The medial division of the medial geniculate body of the cat: implications for thalamic organization , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Jeffrey P. Pascoe,et al.  Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit , 1985, Behavioural Brain Research.

[24]  Michael B. Calford,et al.  The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Michael Davis,et al.  Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala , 1990, Nature.

[26]  Michael B. Calford,et al.  Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  R. Dantzer The Psychology of Fear and Stress, J.A. Gray (Ed.). Cambridge University Press, Cambridge (1987), viii and 422 pp, ISBN 0-521-27098-7 , 1989 .

[28]  Joseph E LeDoux,et al.  Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[31]  Joseph E LeDoux Information flow from sensation to emotion: Plasticity in the neural computation of stimulus value. , 1990 .

[32]  M. Herkenham,et al.  Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing , 1991, The Journal of comparative neurology.

[33]  B. Jacobs,et al.  Participation of the amygdala in complex stimulus recognition and behavioral inhibition: evidence from unit studies. , 1972, Brain research.

[34]  M. Knuepfer,et al.  Sensory input to single neurons in the amygdala of the cat , 1987, Experimental Neurology.

[35]  M. Gabriel,et al.  Learning and Computational Neuroscience: Foundations of Adaptive Networks , 1990 .

[36]  J. O’Keefe,et al.  Complex swnsory properties of certain amygadala units in the freely moving cat. , 1969, Experimental neurology.

[37]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

[38]  Michael Davis,et al.  Anxiety and the Amygdala: Pharmacological and Anatomical Analysis of the Fear-Potentiated Startle Paradigm , 1988 .

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

[40]  W. R. Webster,et al.  Auditory representation within principal division of cat medial geniculate body: an electrophysiology study. , 1981, Journal of neurophysiology.

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