Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body.

Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. Presently little is known about what basic synaptic and cellular mechanisms are employed by thalamocortical neurons in the two main divisions of the auditory thalamus to elicit their distinct responses to sound. Using intracellular recording and labeling methods, we characterized anatomic features, membrane properties, and synaptic inputs of thalamocortical neurons in the dorsal (MGD) and ventral (MGV) divisions in brain slices of rat medial geniculate body. Quantitative analysis of dendritic morphology demonstrated that tufted neurons in both divisions had shorter dendrites, smaller dendritic tree areas, more profuse branching, and a greater dendritic polarization compared with stellate neurons, which were only found in MGD. Tufted neuron dendritic polarization was not as strong or consistent as earlier Golgi studies suggested. MGV and MGD cells had similar intrinsic properties except for an increased prevalence of a depolarizing sag potential in MGV neurons. The sag was the only intrinsic property correlated with cell morphology, seen only in tufted neurons in either division. Many MGV and MGD neurons received excitatory and inhibitory inferior colliculus (IC) inputs (designated IN/EX or EX/IN depending on excitation/inhibition sequence). However, a significant number only received excitatory inputs (EX/O) and a few only inhibitory (IN/O). Both MGV and MGD cells displayed similar proportions of response combinations, but suprathreshold EX/O responses only were observed in tufted neurons. Excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) had multiple distinguishable amplitude levels implying convergence. Excitatory inputs activated alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-D-aspartate (NMDA) receptors the relative contributions of which were variable. For IN/EX cells with suprathreshold inputs, first-spike timing was independent of membrane potential unlike that of EX/O cells. Stimulation of corticothalamic (CT) and thalamic reticular nucleus (TRN) axons evoked a GABAA IPSP, EPSP, GABAB IPSP sequence in most neurons with both morphologies in both divisions. TRN IPSPs and CT EPSPs were graded in amplitude, again suggesting convergence. CT inputs activated AMPA and NMDA receptors. The NMDA component of both IC and CT inputs had an unusual voltage dependence with a detectable DL-2-amino-5-phosphonovaleric acid-sensitive component even below -70 mV. First-spike latencies of CT evoked action potentials were sensitive to membrane potential regardless of whether the TRN IPSP was present. Overall, our in vitro data indicate that reported regional differences in the in vivo responses of MGV and MGD cells to auditory stimuli are not well correlated with major differences in intrinsic membrane features or synaptic responses between cell types.

[1]  M. Steriade,et al.  Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. , 1998, Journal of neurophysiology.

[2]  S. Erulkar,et al.  SYNAPTIC MECHANISMS OF EXCITATION AND INHIBITION IN THE CENTRAL AUDITORY PATHWAY. , 1963, Journal of neurophysiology.

[3]  M. Deschenes,et al.  Corticothalamic Projections from the Cortical Barrel Field to the Somatosensory Thalamus in Rats: A Single‐fibre Study Using Biocytin as an Anterograde Tracer , 1995, The European journal of neuroscience.

[4]  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.

[5]  E. Rouiller,et al.  Origin of afferents to physiologically defined regions of the medial geniculate body of the cat: ventral and dorsal divisions , 1985, Hearing Research.

[6]  Edward L. Bartlett,et al.  A Monosynaptic GABAergic Input from the Inferior Colliculus to the Medial Geniculate Body in Rat , 1997, The Journal of Neuroscience.

[7]  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.

[8]  Morest Dk The neuronal architecture of the medial geniculate body of the cat , 1964 .

[9]  B. Hu,et al.  Lemniscal and non‐lemniscal synaptic transmission in rat auditory thalamus. , 1994, The Journal of physiology.

[10]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[11]  V. Crunelli,et al.  Membrane properties of morphologically identified X and Y cells in the lateral geniculate nucleus of the cat in vitro. , 1987, The Journal of physiology.

[12]  V. Senatorov,et al.  Differential Na+–K+‐ATPase activity in rat lemniscal and non ‐ lemniscal auditory Thalami , 1997, The Journal of physiology.

[13]  G. Aghajanian,et al.  Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices , 1989, Synapse.

[14]  J. Coleman,et al.  Postnatal cytoarchitecture of the rat medial geniculate body , 1998, The Journal of comparative neurology.

[15]  T. Powell,et al.  An electron microscopic study of the mode of termination of cortico-thalamic fibres within the sensory relay nuclei of the thalamus , 1969, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[16]  M. Kudo,et al.  Ascending projections of the inferior colliculus in the cat: An autoradiographic study , 1980, The Journal of comparative neurology.

[17]  D. McCormick,et al.  Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. , 1991, Journal of neurophysiology.

[18]  J. Coleman,et al.  Anatomy of the rat medial geniculate body: I. Cytoarchitecture, myeloarchitecture, and neocortical connectivity , 1990, The Journal of comparative neurology.

[19]  Stephen R. Williams,et al.  Morphology and membrane properties of neurones in the cat ventrobasal thalamus in Vitro , 1997, The Journal of physiology.

[20]  T. Salt,et al.  Role of N-methyl-d-aspartate and metabotropic glutamate receptors in corticothalamic excitatory postsynaptic potentials In vivo , 1996, Neuroscience.

[21]  D. A. McCormick,et al.  Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus , 1995, Neuroscience.

[22]  D. K. Morest,et al.  The lateral tegmental system of the midbrain and the medial geniculate body: Study with Golgi and Nauta methods in cat. , 1965, Journal of anatomy.

[23]  D. Contreras,et al.  Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. , 1996, The Journal of physiology.

[24]  P Heggelund,et al.  Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. II. Nonlagged cells. , 1990, Journal of neurophysiology.

[25]  N. Suga,et al.  Corticofugal modulation of frequency processing in bat auditory system , 1997, Nature.

[26]  L. Aitkin,et al.  Medial geniculate body: unit responses in the awake cat. , 1974, Journal of neurophysiology.

[27]  D. Mooney,et al.  The electrogenic effects of Na+–K+‐ATPase in rat auditory thalamus , 1997, The Journal of physiology.

[28]  N Suga,et al.  Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. , 1997, Journal of neurophysiology.

[29]  M. Sur,et al.  Morphology of retinal axon arbors induced to arborize in a novel target, the medial geniculate nucleus. II. Comparison with axons from the inferior colliculus , 1994, The Journal of comparative neurology.

[30]  E. Welker,et al.  Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex , 1995, Hearing Research.

[31]  D. Coulter,et al.  Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. , 1997, Journal of neurophysiology.

[32]  I. Soltesz,et al.  Sensory input and burst firing output of rat and cat thalamocortical cells: the role of NMDA and non‐NMDA receptors. , 1994, The Journal of physiology.

[33]  E. G. Jones,et al.  Some aspects of the organization of the thalamic reticular complex , 2004, The Journal of comparative neurology.

[34]  M. Sur,et al.  Retinogeniculate EPSPs recorded intracellularly in the ferret lateral geniculate nucleus in vitro: Role of NMDA receptors , 1992, Visual Neuroscience.

[35]  Martin Deschênes,et al.  Electrophysiology and Pharmacology of the Corticothalamic Input to Lateral Thalamic Nuclei: an Intracellular Study in the Cat , 1990, The European journal of neuroscience.

[36]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

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

[38]  N. Weinberger,et al.  Corticofugal modulation of the medial geniculate body , 1976, Experimental Neurology.

[39]  J. Winer,et al.  Anatomy of glutamic acid decarboxylase immunoreactive neurons and axons in the rat medial geniculate body , 1988, The Journal of comparative neurology.

[40]  J. Adams Heavy metal intensification of DAB-based HRP reaction product. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[41]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[42]  C. Koch,et al.  Constraints on cortical and thalamic projections: the no-strong-loops hypothesis , 1998, Nature.

[43]  A. Wenzel,et al.  Distribution of NMDA receptor subunit proteins NR2A, 2B, 2C and 2D in rat brain , 1995, Neuroreport.

[44]  D. McCormick,et al.  Properties of a hyperpolarization‐activated cation current and its role in rhythmic oscillation in thalamic relay neurones. , 1990, The Journal of physiology.

[45]  A. McDonald,et al.  Anatomy of the rat medial geniculate body: II. Dendritic morphology , 1990, The Journal of comparative neurology.

[46]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[47]  S. Sherman,et al.  Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode , 1995, Visual Neuroscience.

[48]  J. Winer,et al.  The neuronal architecture of the dorsal division of the medial geniculate body of the cat. A study with the rapid Golgi method , 1983, The Journal of comparative neurology.

[49]  M. Kudo,et al.  Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques , 1978, Brain Research.

[50]  D. McCormick Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity , 1992, Progress in Neurobiology.

[51]  A. Rees,et al.  Ascending Projections to the Medial Geniculate Body from Physiologically Identified Loci in the Inferior Colliculus , 1997 .

[52]  M. Merzenich,et al.  The efferent projections of the central nucleus and the pericentral nucleus of the inferior collculus in the cat , 1980, The Journal of comparative neurology.

[53]  D. Paré,et al.  Three types of inhibitory postsynaptic potentials generated by interneurons in the anterior thalamic complex of cat. , 1991, Journal of neurophysiology.

[54]  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.

[55]  R. L. Marie,et al.  Substrate for rapid feedforward inhibition of the auditory forebrain , 1997, Brain Research.

[56]  S B Nelson,et al.  Effect of stimulus contrast and size on NMDA receptor activity in cat lateral geniculate nucleus. , 1992, Journal of neurophysiology.

[57]  E. Puil,et al.  Mechanisms for signal transformation in lemniscal auditory thalamus. , 1996, Journal of neurophysiology.

[58]  J. Crabtree Organization in the auditory sector of the cat's thalamic reticular nucleus , 1998 .

[59]  Muscarine induces an anomalous inhibition of synaptic transmission in rat auditory thalamic neurons in vitro. , 1995, The Journal of pharmacology and experimental therapeutics.

[60]  Thierry Bal,et al.  Sensory gating mechanisms of the thalamus , 1994, Current Opinion in Neurobiology.

[61]  E. Welker,et al.  Morphology of corticothalamic terminals arising from the auditory cortex of the rat: A Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study , 1991, Hearing Research.

[62]  D. Frost,et al.  Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: Target‐controlled morphogenesis of axon terminals and synaptic glomeruli , 1988, The Journal of comparative neurology.

[63]  M. Pirchio,et al.  The ventral and dorsal lateral geniculate nucleus of the rat: intracellular recordings in vitro. , 1987, The Journal of physiology.

[64]  T. Imig,et al.  Tonotopic organization in ventral nucleus of medial geniculate body in the cat. , 1985, Journal of neurophysiology.

[65]  Morest Dk The lateral tegmental system of the midbrain and the medial geniculate body: Study with Golgi and Nauta methods in cat , 1965 .

[66]  Richard R. Fay,et al.  The Mammalian Auditory Pathway: Neuroanatomy , 1992, Springer Handbook of Auditory Research.

[67]  P. Heggelund,et al.  Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. I. Lagged cells. , 1990, Journal of neurophysiology.

[68]  D. Irvine Physiology of the Auditory Brainstem , 1992 .

[69]  A. Agmon,et al.  Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro. , 1994, Journal of neurophysiology.

[70]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

[71]  J. Winer The Functional Architecture of the Medial Geniculate Body and the Primary Auditory Cortex , 1992 .

[72]  N Suga,et al.  Corticofugal Modulation of Time-Domain Processing of Biosonar Information in Bats , 1996, Science.

[73]  D. Kent Morest,et al.  Axons of the dorsal division of the medial geniculate body of the cat: A study with the rapid Golgi method , 1984, The Journal of comparative neurology.

[74]  David A. McCormick,et al.  Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current , 1989, Nature.

[75]  B. Sakmann,et al.  Developmental and regional expression in the rat brain and functional properties of four NMDA receptors , 1994, Neuron.

[76]  W. R. Webster,et al.  Tonotopic organization in the medial geniculate body of the cat. , 1971, Brain research.

[77]  R. Guillery Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. , 1995, Journal of anatomy.

[78]  D. Contreras,et al.  Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. , 1998, Journal of neurophysiology.

[79]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

[80]  B. Hu Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. , 1995, The Journal of physiology.

[81]  Morest Dk THE LAMINAR STRUCTURE OF THE MEDIAL GENICULATE BODY OF THE CAT. , 1965 .

[82]  P. Ohara,et al.  Preserved features of thalamocortical projection neuron dendritic architecture in the somatosensory thalamus of the rat, cat and macaque , 1994, Brain Research.

[83]  R. Pearce,et al.  Hyperpolarization-activated cation current (Ih) in neurons of the medial nucleus of the trapezoid body: voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. , 1993, Journal of neurophysiology.

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

[85]  Modulation of bursts and high-threshold calcium spikes in neurons of rat auditory thalamus , 1998, Neuroscience.

[86]  H. Ojima Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. , 1994, Cerebral cortex.

[87]  A. Wenzel,et al.  NMDA Receptor Heterogeneity During Postnatal Development of the Rat Brain: Differential Expression of the NR2A, NR2B, and NR2C Subunit Proteins , 1997, Journal of neurochemistry.

[88]  Pascal Barone,et al.  Physiology of Thalamus and Cortex , 1992 .

[89]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[90]  W. Guido,et al.  Burst responses in thalamic relay cells of the awake behaving cat. , 1995, Journal of neurophysiology.

[91]  N Suga,et al.  Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. , 1997, Journal of neurophysiology.

[92]  P. Smith Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  J. Winer,et al.  GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[94]  W. R. Webster,et al.  Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. , 1972, Journal of neurophysiology.

[95]  E. Rouiller,et al.  Projections of the reticular complex of the thalamus onto physiologically characterized regions of the medial geniculate body , 1985, Neuroscience Letters.

[96]  D. McCormick,et al.  Noradrenergic and serotonergic modulation of a hyperpolarization‐activated cation current in thalamic relay neurones. , 1990, The Journal of physiology.

[97]  M. Steriade Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. , 1997, Cerebral cortex.

[98]  R E Weller,et al.  Structural correlates of functionally distinct X‐cells in the lateral geniculate nucleus of the cat , 1988, The Journal of comparative neurology.

[99]  T. Powell,et al.  Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat , 1969, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[100]  N. Mizuno,et al.  Distrubution and size of thalamic neurons projecting to layer I of the auditory cortical fields of the cat compared to those projecting to layer IV , 1987, The Journal of comparative neurology.

[101]  D. McCormick,et al.  Periodicity of Thalamic Synchronized Oscillations: the Role of Ca2+-Mediated Upregulation of Ih , 1998, Neuron.