Anatomic, Intrinsic, and Synaptic Properties of Dorsal and Ventral Division Neurons in Rat Medial Geniculate Body

1999 ◽  
Vol 81 (5) ◽  
pp. 1999-2016 ◽  
Author(s):  
Edward L. Bartlett ◽  
Philip H. Smith

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 α-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.

2008 ◽  
Vol 99 (6) ◽  
pp. 2938-2945 ◽  
Author(s):  
Zhuo Zhang ◽  
Chun-Hua Liu ◽  
Yan-Qin Yu ◽  
Kenji Fujimoto ◽  
Ying-Shing Chan ◽  
...  

Electrical stimulation of the auditory cortex (AC) causes both facilitatory and inhibitory effects on the medial geniculate body (MGB). The purpose of this study was to identify the corticofugal inhibitory pathway to the MGB. We assessed two potential circuits: 1) the cortico-colliculo-thalamic circuit and 2) cortico-reticulo-thalamic one. We compared intracellular responses of MGB neurons to electrical stimulation of the AC following bilateral ablation of the inferior colliculi (IC) or thalamic reticular nucleus (TRN) in anesthetized guinea pigs. Cortical stimulation with intact TRN could cause strong inhibitory effects on the MGB neurons. The corticofugal inhibition remained effective after bilateral IC ablation, but it was minimized after the TRN was lesioned with kainic acid. Synchronized TRN neuronal activity and MGB inhibitory postsynaptic potentials (IPSPs) were observed with multiple recordings. The results suggest that corticofugal inhibition traverses the corticoreticulothalamic pathway, indicating that the colliculi-geniculate inhibitory pathway is probably only for feedforward inhibition.


2007 ◽  
Vol 58 ◽  
pp. S156
Author(s):  
Akihisa Kimura ◽  
Tomohiro Donishi ◽  
Hiroki Imbe ◽  
Yasuhiko Tamai

2021 ◽  
Vol 15 ◽  
Author(s):  
Natsumi Y. Homma ◽  
Victoria M. Bajo

Sound information is transmitted from the ear to central auditory stations of the brain via several nuclei. In addition to these ascending pathways there exist descending projections that can influence the information processing at each of these nuclei. A major descending pathway in the auditory system is the feedback projection from layer VI of the primary auditory cortex (A1) to the ventral division of medial geniculate body (MGBv) in the thalamus. The corticothalamic axons have small glutamatergic terminals that can modulate thalamic processing and thalamocortical information transmission. Corticothalamic neurons also provide input to GABAergic neurons of the thalamic reticular nucleus (TRN) that receives collaterals from the ascending thalamic axons. The balance of corticothalamic and TRN inputs has been shown to refine frequency tuning, firing patterns, and gating of MGBv neurons. Therefore, the thalamus is not merely a relay stage in the chain of auditory nuclei but does participate in complex aspects of sound processing that include top-down modulations. In this review, we aim (i) to examine how lemniscal corticothalamic feedback modulates responses in MGBv neurons, and (ii) to explore how the feedback contributes to auditory scene analysis, particularly on frequency and harmonic perception. Finally, we will discuss potential implications of the role of corticothalamic feedback in music and speech perception, where precise spectral and temporal processing is essential.


1990 ◽  
Vol 297 (1) ◽  
pp. 32-54 ◽  
Author(s):  
William J. Clerici ◽  
Alexander J. McDonald ◽  
Richard Thompson ◽  
James R. Coleman

2013 ◽  
Vol 109 (12) ◽  
pp. 2866-2882 ◽  
Author(s):  
Yamini Venkataraman ◽  
Edward L Bartlett

The development of auditory temporal processing is important for processing complex sounds as well as for acquiring reading and language skills. Neuronal properties and sound processing change dramatically in auditory cortex neurons after the onset of hearing. However, the development of the auditory thalamus or medial geniculate body (MGB) has not been well studied over this critical time window. Since synaptic inhibition has been shown to be crucial for auditory temporal processing, this study examined the development of a feedforward, GABAergic connection to the MGB from the inferior colliculus (IC), which is also the source of sensory glutamatergic inputs to the MGB. IC-MGB inhibition was studied using whole cell patch-clamp recordings from rat brain slices in current-clamp and voltage-clamp modes at three age groups: a prehearing group [ postnatal day (P)7–P9], an immediate posthearing group (P15–P17), and a juvenile group (P22–P32) whose neuronal properties are largely mature. Membrane properties matured substantially across the ages studied. GABAA and GABAB inhibitory postsynaptic potentials were present at all ages and were similar in amplitude. Inhibitory postsynaptic potentials became faster to single shocks, showed less depression to train stimuli at 5 and 10 Hz, and were overall more efficacious in controlling excitability with age. Overall, IC-MGB inhibition becomes faster and more precise during a time period of rapid changes across the auditory system due to the codevelopment of membrane properties and synaptic properties.


1994 ◽  
Vol 72 (2) ◽  
pp. 1032-1036 ◽  
Author(s):  
M. R. Pelletier ◽  
J. J. Hablitz

1. Neocortical brain slices were prepared from rats (35–50 days of age) and maintained in vitro. Intracellular recordings were obtained from neurons in cortical layers II/III. The effect of bath application of cyclothiazide (CYZ), a potent blocker of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor desensitization, on evoked synaptic activity and passive membrane properties was investigated. 2. Bath application of CYZ did not significantly affect resting membrane potential, input resistance, or repetitive firing. CYZ increased both the amplitude and duration of evoked excitatory postsynaptic potentials (EPSPs). Polysynaptic responses were also augumented. These effects persisted after the blockade of N-methyl-D-aspartate (NMDA) receptors with D-2-amino-5-phosphonovaleric acid (D-APV). The magnitude of these effects appeared to vary directly with stimulation intensity and presumably, amount of glutamate release. 3. Epileptiform activity was induced by bath application of bicuculline methiodide. The amplitude and duration of evoked paroxysmal discharges were increased by CYZ. Similar results were seen in presence of D-APV. 4. These results indicate that CYZ has significant effects on synaptic transmission. Desensitization of non-NMDA receptors may be an important mechanism for determining the time course of EPSPs and in curtailing epileptiform responses in the rat neocortex.


2001 ◽  
Vol 86 (3) ◽  
pp. 1252-1265 ◽  
Author(s):  
Yu-Feng Wang ◽  
Xiao-Bing Gao ◽  
Anthony N. van den Pol

Spikes may play an important role in modulating a number of aspects of brain development. In early hypothalamic development, GABA can either evoke action potentials, or it can shunt other excitatory activity. In both slices and cultures of the mouse hypothalamus, we observed a heterogeneity of spike patterns and frequency in response to GABA. To examine the mechanisms underlying patterns and frequency of GABA-evoked spikes, we used conventional whole cell and gramicidin perforation recordings of neurons ( n = 282) in slices and cultures of developing mouse hypothalamus. Recorded with gramicidin pipettes, GABA application evoked action potentials in hypothalamic neurons in brain slices of postnatal day 2–9( P2- 9) mice. With conventional patch pipettes (containing 29 mM Cl−), action potentials were also elicited by GABA from neurons of 2–13 days in vitro (2–13 DIV) embryonic hypothalamic cultures. Depolarizing responses to GABA could be generally classified into three types: depolarization with no spike, a single spike, or complex patterns of multiple spikes. In parallel experiments in slices, electrical stimulation of GABAergic mediobasal hypothalamic neurons in the presence of glutamate receptor antagonists [10 μM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), 100 μM 2-amino-5-phosphonopentanoic acid (AP5)] resulted in the occurrence of spikes that were blocked by bicuculline (20 μM). Blocking ionotropic glutamate receptors with AP5 and CNQX did not block GABA-mediated multiple spikes. Similarly, when synaptic transmission was blocked with Cd2+ (200 μM) and Ni2+(300 μM), GABA still induced multiple spikes, suggesting that the multiple spikes can be an intrinsic membrane property of GABA excitation and were not based on local interneurons. When the pipette [Cl−] was 29 or 45 mM, GABA evoked multiple spikes. In contrast, spikes were not detected with 2 or 10 mM intracellular [Cl−]. With gramicidin pipettes, we found that the mean reversal potential of GABA-evoked current ( E GABA) was positive to the resting membrane potential, suggesting a high intracellular [Cl−] in developing mouse neurons. Varying the holding potential from −80 to 0 mV revealed an inverted U-shaped effect on spike probability. Blocking voltage-dependent Na+ channels with tetrodotoxin eliminated GABA-evoked spikes, but not the GABA-evoked depolarization. Removing Ca2+ from the extracellular solution did not block spikes, indicating GABA-evoked Na+-based spikes. Although E GABA was more positive within 2–5 days in culture, the probability of GABA-evoked spikes was greater in 6- to 9-day cells. Mechanistically, this appears to be due to a greater Na+ current found in the older cells during a period when the E GABA is still positive to the resting membrane potential. GABA evoked similar spike patterns in HEPES and bicarbonate buffers, suggesting that Cl−, not bicarbonate, was primarily responsible for generatingmultiple spikes. GABA evoked either single or multiple spikes; neurons with multiple spikes had a greater Na+ current, a lower conductance, a more negative spike threshold, and a greater difference between the peak of depolarization and the spike threshold. Taken together, the present results indicate that the patterns of multiple action potentials evoked by GABA are an inherent property of the developing hypothalamic neuron.


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