Opposite effects of tetanic stimulation of the auditory thalamus or auditory cortex on the acoustic startle reflex in awake rats

The amygdala mediates both emotional learning and fear potentiation of startle. The lateral amygdala nucleus (LA) receives auditory inputs from both the auditory thalamus (medial geniculate nucleus; MGN) and auditory association cortex (AAC), and is critical for auditory fear conditioning. The central amygdala nucleus, which has intra‐amygdaloid connections with LA, enhances startle magnitude via midbrain connections to the startle circuits. Tetanic stimulation of either MGN or AAC in vitro or in vivo can induce long‐term potentiation in LA. In the present study, behavioural consequences of tetanization of these auditory afferents were investigated in awake rats. The acoustic startle reflex of rats was enhanced by tetanic stimulation of MGN, but suppressed by that of AAC. All the tetanization‐induced changes of startle diminished within 24 h. Blockade of GABAB receptors in the LA area reversed the suppressive effect of tetanic stimulation of AAC on startle but did not change the enhancing effect of tetanic stimulation of MGN. Moreover, transient electrical stimulation of MGN enhanced the acoustic startle reflex when it lagged behind acoustic stimulation, but inhibited the acoustic startle reflex when it preceded acoustic stimulation. The results of the present study indicate that MGN and AAC afferents to LA play different roles in emotional modulation of startle, and AAC afferents are more influenced by inhibitory GABAB transmission in LA.

[1]  M. Davis,et al.  Using pavlovian higher-order conditioning paradigms to investigate the neural substrates of emotional learning and memory. , 2000, Learning & memory.

[2]  L. Li,et al.  Contributions of the vestibular nucleus and vestibulospinal tract to the startle reflex , 2001, Neuroscience.

[3]  H. C. Moises,et al.  Inhibitory responses of rat basolateral amygdaloid neurons recorded in vitro , 1992, Neuroscience.

[4]  Joseph E. LeDoux,et al.  Extinction of emotional learning: Contribution of medial prefrontal cortex , 1993, Neuroscience Letters.

[5]  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.

[6]  M. McKERNAN,et al.  Comparison of paired‐pulse facilitation of AMPA and NMDA synaptic currents in the lateral amygdala , 2001, Synapse.

[7]  Liang Li,et al.  Restricted lesions to ventral prefrontal subareas block reversal learning but not visual discrimination learning in rats , 1998, Physiology & Behavior.

[8]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

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

[10]  Joseph E LeDoux,et al.  Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala , 2000, Synapse.

[11]  J. Yeomans,et al.  Effects of bilateral electrical stimulation of the ventral pallidum on acoustic startle , 1999, Brain Research.

[12]  E. Meloni,et al.  Muscimol in the deep layers of the superior colliculus/mesencephalic reticular formation blocks expression but not acquisition of fear-potentiated startle in rats. , 1999, Behavioral neuroscience.

[13]  G. Quirk,et al.  The Role of Ventromedial Prefrontal Cortex in the Recovery of Extinguished Fear , 2000, The Journal of Neuroscience.

[14]  Joseph E LeDoux,et al.  Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat , 1995, Neuron.

[15]  E. Meloni,et al.  GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D1 Receptor Agonist SKF 82958 in Rats , 2000, The Journal of Neuroscience.

[16]  H. Pape,et al.  Putative Cortical and Thalamic Inputs Elicit Convergent Excitation in a Population of GABAergic Interneurons of the Lateral Amygdala , 2000, The Journal of Neuroscience.

[17]  Joseph E. LeDoux,et al.  LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit , 1995, Neuron.

[18]  Chiung‐Chun Huang,et al.  Paired‐pulse depression of the N‐methyl‐D‐aspartate receptor‐mediated synaptic potentials in the amygdala , 1994, British journal of pharmacology.

[19]  Michael Davis,et al.  Enhancement of the acoustic startle response in rats by the dopamine D1 receptor agonist SKF 82958 , 1999, Psychopharmacology.

[20]  J. R. Augustine,et al.  Localization of GABA-like immunoreactivity in the monkey amygdala , 1993, Neuroscience.

[21]  P. Sah,et al.  Excitatory synaptic inputs to pyramidal neurons of the lateral amygdala , 1999, European Journal of Neuroscience.

[22]  D. Paré,et al.  Stimulation of Medial Prefrontal Cortex Decreases the Responsiveness of Central Amygdala Output Neurons , 2003, The Journal of Neuroscience.

[23]  Joseph E LeDoux,et al.  Ultrastructure and synaptic associations of auditory thalamo-amygdala projections in the rat , 2004, Experimental Brain Research.

[24]  Joseph E LeDoux,et al.  A gradient of plasticity in the amygdala revealed by cortical and subcortical stimulation, in vivo , 2001, Neuroscience.

[25]  Stephen Maren.  Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits. , 1996, Molecular neurobiology.

[26]  E. Asprodini,et al.  Excitatory transmission in the basolateral amygdala. , 1991, Journal of neurophysiology.

[27]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[28]  J. S Yeomans,et al.  Summation between acoustic and trigeminal stimuli evoking startle , 1999, Neuroscience.

[29]  Joseph E LeDoux,et al.  Heterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala , 2004, The Journal of Neuroscience.

[30]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[31]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Koch,et al.  Corticotropin‐releasing Factor in the Caudal Pontine Reticular Nucleus Mediates the Expression of Fear‐potentiated Startle in the Rat , 1997, The European journal of neuroscience.

[33]  Joseph E LeDoux,et al.  NMDA and AMPA receptors in the lateral nucleus of the amygdala are postsynaptic to auditory thalamic afferents , 1997, Synapse.

[34]  M. Jung,et al.  Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. , 2001, Cerebral cortex.

[35]  J. S. Brown,et al.  Conditioned fear as revealed by magnitude of startle response to an auditory stimulus. , 1951, Journal of experimental psychology.

[36]  P. Sah,et al.  Excitatory Synaptic Transmission in the Lateral and Central Amygdala , 2003, Annals of the New York Academy of Sciences.

[37]  G. Quirk,et al.  Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. , 2004, Behavioral neuroscience.

[38]  Michael Davis,et al.  Enhancement of electrically elicited startle by amygdaloid stimulation , 1990, Physiology & Behavior.

[39]  T. Blumenthal,et al.  The startle response as an indicator of temporal summation , 1986, Perception & psychophysics.

[40]  M. Koch,et al.  Lesions of the central gray block the sensitization of the acoustic startle response in rats , 1994, Brain Research.

[41]  T. Insel,et al.  Subcortical projections of area 25 (subgenual cortex) of the macaque monkey , 2000, The Journal of comparative neurology.

[42]  Temporal integration in the acoustic startle reflex of the rat. , 1973, Journal of comparative and physiological psychology.

[43]  D. Mcintyre,et al.  Another inexpensive headplug for the electrical recording and or stimulation of rats. , 1972, Physiology & behavior.

[44]  Pankaj Sah,et al.  Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala , 1998, Nature.

[45]  E. Tsvetkov,et al.  Glutamate Uptake Determines Pathway Specificity of Long-Term Potentiation in the Neural Circuitry of Fear Conditioning , 2004, Neuron.

[46]  Y. Ikegaya,et al.  Roles of GABAA, NMDA and muscarinic receptors in induction of long-term potentiation in the medial and lateral amygdala in vitro , 1995, Neuroscience Research.

[47]  Theresa M. Desrochers,et al.  Two different lateral amygdala cell populations contribute to the initiation and storage of memory , 2001, Nature Neuroscience.

[48]  A. McDonald.  Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat , 1982, The Journal of comparative neurology.

[49]  D. Paré,et al.  Synaptic responsiveness of interneurons of the cat lateral amygdaloid nucleus , 1998, Neuroscience.

[50]  R. North,et al.  Membrane properties and synaptic potentials of three types of neurone in rat lateral amygdala. , 1993, The Journal of physiology.

[51]  Joseph E LeDoux,et al.  Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. , 1996, Learning & memory.

[52]  J. Yeomans,et al.  Enhancement of electrically evoked startle-like responses by tetanic stimulation of the superior colliculus , 2002, Neuroreport.

[53]  Michael Davis,et al.  The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety. , 1992, Trends in pharmacological sciences.

[54]  E. Asprodini,et al.  Inhibitory transmission in the basolateral amygdala. , 1991, Journal of neurophysiology.

[55]  N. Swerdlow,et al.  Startle response models of sensorimotor gating and habituation deficits in schizophrenia , 1990, Brain Research Bulletin.

[56]  Stephen Maren,et al.  Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. , 2001, Learning & memory.

[57]  F. Mascagni,et al.  Corticoamygdaloid and corticocortical projections of the rat temporal cortex: APhaseolus vulgaris leucoagglutinin study , 1993, Neuroscience.

[58]  L. Li,et al.  Prepulse inhibition of acoustic or trigeminal startle of rats by unilateral electrical stimulation of the inferior colliculus. , 1998, Behavioral neuroscience.

[59]  F. Mascagni,et al.  Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat , 1996, Neuroscience.

[60]  David M. Smith,et al.  Medial Geniculate, Amygdalar and Cingulate Cortical Training-Induced Neuronal Activity during Discriminative Avoidance Learning in Rabbits with Auditory Cortical Lesions , 2001, Journal of Neuroscience.

[61]  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.

[62]  H. Hoffman,et al.  Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. , 1980, Psychological review.

[63]  Joseph E LeDoux,et al.  Afferents from rat temporal cortex synapse on lateral amygdala neurons that express NMDA and AMPA receptors , 1999, Synapse.

[64]  M. Fendt,et al.  The neuroanatomical and neurochemical basis of conditioned fear , 1999, Neuroscience & Biobehavioral Reviews.

[65]  D. Paré,et al.  Similar inhibitory processes dominate the responses of cat lateral amygdaloid projection neurons to their various afferents. , 1997, Journal of neurophysiology.

[66]  T. Powell,et al.  The projection of the auditory cortex upon the diencephalon and brain stem in the cat. , 1969, Brain research.

[67]  M. Koch.  Microinjections of the metabotropic glutamate receptor agonist,trans-(±)-1-amino-cyclopentane-1,3-dicarboxylate (trans-ACPD) into the amygdala increase the acoustic startle response of rats , 1993, Brain Research.

[68]  Eric R Kandel,et al.  Postsynaptic Induction and PKA-Dependent Expression of LTP in the Lateral Amygdala , 1998, Neuron.

[69]  Joseph E LeDoux,et al.  NMDA Receptors and L-Type Voltage-Gated Calcium Channels Contribute to Long-Term Potentiation and Different Components of Fear Memory Formation in the Lateral Amygdala , 2002, The Journal of Neuroscience.

[70]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[71]  Liang Li,et al.  Tactile, acoustic and vestibular systems sum to elicit the startle reflex , 2002, Neuroscience & Biobehavioral Reviews.

[72]  Joseph E LeDoux,et al.  Intra-Amygdala Blockade of the NR2B Subunit of the NMDA Receptor Disrupts the Acquisition But Not the Expression of Fear Conditioning , 2001, The Journal of Neuroscience.

[73]  J. Yeomans,et al.  Double-pulse stimulation of startle-like responses in rats: refractory periods and temporal summation , 1989, Brain Research.

[74]  Joseph E LeDoux,et al.  Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat , 1999, The Journal of comparative neurology.

[75]  Amygdala efferents mediating electrically evoked startle-like responses and fear potentiation of acoustic startle. , 1993, Behavioral neuroscience.

[76]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[77]  M. Davis,et al.  Enhancement of acoustic startle by electrical stimulation of the amygdala. , 1988, Behavioral neuroscience.

[78]  L. Li,et al.  Using intracranial electrical stimulation to study the timing of prepulse inhibition of the startle reflex. , 2000, Brain research. Brain research protocols.

[79]  O. E. Millhouse,et al.  Neuronal configurations in lateral and basolateral amygdala , 1983, Neuroscience.

[80]  K. Sripanidkulchai,et al.  The cortical projection of the basolateral amygdaloid nucleus in the rat: A retrograde fluorescent dye study , 1984, The Journal of comparative neurology.

[81]  M. Koch,et al.  Lesions of the Amygdala Do Not Affect the Enhancement of the Acoustic Startle Response by Background Noise , 1996, Physiology & Behavior.

[82]  H. Okaichi,et al.  Effect of lesions in the lateral nucleus of the amygdala on fear conditioning using auditory and visual conditioned stimuli in rats , 2002, Neuroscience Research.

[83]  Liang Li,et al.  Glutamate and GABAB transmissions in lateral amygdala are involved in startle-like electromyographic (EMG) potentiation caused by activation of auditory thalamus , 2005, Neuroscience Letters.

[84]  E. W. Kairiss,et al.  Long-term synaptic potentiation. , 1988, Science.

[85]  Joseph E LeDoux,et al.  Distinct populations of NMDA receptors at subcortical and cortical inputs to principal cells of the lateral amygdala. , 1999, Journal of neurophysiology.

[86]  M. Fendt,et al.  Amygdaloid N-methyl-d-aspartate and γ-aminobutyric acidA receptors regulate sensorimotor gating in a dopamine-dependent way in rats , 2000, Neuroscience.

[87]  Michael Koch,et al.  Enhancement of the acoustic startle response by stimulation of an excitatory pathway from the central amygdala/basal nucleus of Meynert to the pontine reticular formation , 2004, Experimental Brain Research.

[88]  Michael Davis,et al.  Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. , 1986, Behavioral neuroscience.

[89]  Fear-potentiated startle and electrically evoked startle mediated by synapses in rostrolateral midbrain. , 1995, Behavioral neuroscience.

[90]  F. Graham,et al.  Presidential Address, 1974. The more or less startling effects of weak prestimulation. , 1975, Psychophysiology.

[91]  D. Amaral,et al.  Organization of the intrinsic connections of the monkey amygdaloid complex: Projections originating in the lateral nucleus , 1998, The Journal of comparative neurology.

[92]  M. Fendt,et al.  Injections of the NMDA Receptor Antagonist Aminophosphonopentanoic Acid into the Lateral Nucleus of the Amygdala Block the Expression of Fear-Potentiated Startle and Freezing , 2001, The Journal of Neuroscience.

[93]  Joseph E LeDoux,et al.  L-Type Voltage-Gated Calcium Channels Mediate NMDA-Independent Associative Long-Term Potentiation at Thalamic Input Synapses to the Amygdala , 1999, The Journal of Neuroscience.

[94]  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.

[95]  Liang Li,et al.  Auditory gating processes and binaural inhibition in the inferior colliculus , 2002, Hearing Research.

[96]  Joseph E LeDoux.  Emotion: clues from the brain. , 1995, Annual review of psychology.

[97]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[98]  M. Koch,et al.  Lesions of the central gray block conditioned fear as measured with the potentiated startle paradigm , 1996, Behavioural Brain Research.

[99]  Y. Ben‐Ari,et al.  Distribution of GABA‐like immunoreactivity in the rat amygdaloid complex , 1987, The Journal of comparative neurology.

[100]  Joseph E LeDoux,et al.  NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala , 1995, Experimental Brain Research.

[101]  J. Yeomans,et al.  Fear-potentiated startle and electrically evoked startle mediated by synapses in rostrolateral midbrain , 1995 .

[102]  N. Weinberger,et al.  Frequency selectivity is related to temporal processing in parallel thalamocortical auditory pathways , 1992, Brain Research.

[103]  S. Royer,et al.  Polarized synaptic interactions between intercalated neurons of the amygdala. , 2000, Journal of neurophysiology.

[104]  H. T. Blair,et al.  Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. , 2001, Learning & memory.

[105]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid projections of rat temporal cortex , 1997, The Journal of comparative neurology.

[106]  H. Hoffman,et al.  Reflex modification in the domain of startle: II. The anomalous history of a robust and ubiquitous phenomenon. , 1983, Psychological bulletin.

[107]  Michael Davis,et al.  The design and calibration of a startle measurement system , 1986, Physiology & Behavior.

[108]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[109]  Torfi Sigurdsson,et al.  Long‐term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala , 2003, The European journal of neuroscience.

[110]  Joseph E LeDoux,et al.  New vistas on amygdala networks in conditioned fear. , 2004, Journal of neurophysiology.

[111]  E. W. Kairiss,et al.  Long‐Term synaptic potentiation in the amygdala , 1990, Synapse.

[112]  A direct projection from the central nucleus of the amygdala to the acoustic startle pathway: anterograde and retrograde tracing studies. , 1991, Behavioral neuroscience.