scholarly journals Learning-related population dynamics in the auditory thalamus

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Ariel Gilad ◽  
Ido Maor ◽  
Adi Mizrahi

Learning to associate sensory stimuli with a chosen action involves a dynamic interplay between cortical and thalamic circuits. While the cortex has been widely studied in this respect, how the thalamus encodes learning-related information is still largely unknown. We studied learning-related activity in the medial geniculate body (MGB; Auditory thalamus), targeting mainly the dorsal and medial regions. Using fiber photometry, we continuously imaged population calcium dynamics as mice learned a go/no-go auditory discrimination task. The MGB was tuned to frequency and responded to cognitive features like the choice of the mouse within several hundred milliseconds. Encoding of choice in the MGB increased with learning, and was highly correlated with the learning curves of the mice. MGB also encoded motor parameters of the mouse during the task. These results provide evidence that the MGB encodes task- motor- and learning-related information.

Author(s):  
Ariel Gilad ◽  
Ido Maor ◽  
Adi Mizrahi

AbstractLearning to associate sensory stimuli with a chosen action has been classically attributed to the cortex. Whether the thalamus, considered mainly as an upstream area relative to cortex, encodes learning-related information is still largely unknown. We studied learning-related activity in the dorsal and medial regions of the medial geniculate body (MGB), part of the non-lemniscal auditory pathway. Using fiber photometry, we continuously imaged population calcium dynamics as mice learned a go/no-go auditory discrimination task. The MGB was tuned to frequency shortly after stimulus onset and responded to cognitive features like the choice of the mouse several hundred milliseconds later. Encoding of choice in the MGB increased with learning, and was highly correlated with the learning curves of the mice. MGB also encoded motor parameters of the mouse during the task. These results provide evidence that the MGB encodes task- motor- and learning-related information.


2002 ◽  
Vol 88 (4) ◽  
pp. 2152-2156 ◽  
Author(s):  
Jufang He ◽  
Bin Hu

The medial geniculate body (MGB) of the auditory thalamus comprises lemniscal and nonlemniscal neurons that project to the primary auditory cortex and limbic structures, respectively. Here we show that in anesthetized guinea pigs, MGB responses to a noise-burst stimulus exhibit distinct and synaptic pathway-specific firing patterns. The majority of nonlemniscal MGB cells exhibited bursting responses, whereas lemniscal neurons discharged mainly single or spike doublets. The burst firing is delayed in nonlemniscal neurons and exhibited several features that are characteristics of those mediated by low-threshold Ca2+ spikes. Such a synaptic pathway-specific allocation of bursting and single-spike firing patterns is consistent with the notion of parallel processing of auditory information in thalamocortical system.


2011 ◽  
Vol 105 (6) ◽  
pp. 2647-2667 ◽  
Author(s):  
Edward L. Bartlett ◽  
Xiaoqin Wang

As the information bottleneck of nearly all auditory input that reaches the cortex, the auditory thalamus serves as the basis for establishing auditory cortical processing streams. The functional organization of the primary and nonprimary subdivisions of the auditory thalamus is not well characterized, particularly in awake primates. We have recorded from neurons in the auditory thalamus of awake marmoset monkeys and tested their responses to tones, band-pass noise, and temporally modulated stimuli. We analyzed the spectral and temporal response properties of recorded neurons and correlated those properties with their locations in the auditory thalamus, thereby forming the basis for parallel output channels. Three medial geniculate body (MGB) subdivisions were identified and studied physiologically and anatomically, although other medial subdivisions were also identified anatomically. Neurons in the ventral subdivision (MGV) were sharply tuned for frequency, preferred narrowband stimuli, and were able to synchronize to rapid temporal modulations. Anterodorsal subdivision (MGAD) neurons appeared well suited for temporal processing, responding similarly to tone or noise stimuli but able to synchronize to the highest modulation frequencies and with the highest temporal precision among MGB subdivisions. Posterodorsal subdivision (MGPD) neurons differed substantially from the other two subdivisions, with many neurons preferring broadband stimuli and signaling changes in modulation frequency with nonsynchronized changes in firing rate. Most neurons in all subdivisions responded to increases in tone sound level with nonmonotonic changes in firing rate. MGV and MGAD neurons exhibited responses consistent with provision of thalamocortical input to core regions, whereas MGPD neurons were consistent with provision of input to belt regions.


2014 ◽  
Vol 111 (2) ◽  
pp. 229-238 ◽  
Author(s):  
Rui Cai ◽  
Bopanna I. Kalappa ◽  
Thomas J. Brozoski ◽  
Lynne L. Ling ◽  
Donald M. Caspary

Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the central auditory system. Sensory thalamic structures show high levels of non-desensitizing extrasynaptic GABAA receptors (GABAARs) and a reduction in the redundancy of coded information. The present study compared the inhibitory potency of GABA acting at GABAARs between the inferior colliculus (IC) and the medial geniculate body (MGB) using quantitative in vivo, in vitro, and ex vivo experimental approaches. In vivo single unit studies compared the ability of half maximal inhibitory concentrations of GABA to inhibit sound-evoked temporal responses, and found that GABA was two to three times ( P < 0.01) more potent at suppressing MGB single unit responses than IC unit responses. In vitro whole cell patch-clamp slice recordings were used to demonstrate that gaboxadol, a δ-subunit selective GABAAR agonist, was significantly more potent at evoking tonic inhibitory currents from MGB neurons than IC neurons ( P < 0.01). These electrophysiological findings were supported by an in vitro receptor binding assay which used the picrotoxin analog [3H]TBOB to assess binding in the GABAAR chloride channel. MGB GABAARs had significantly greater total open chloride channel capacity relative to GABAARs in IC ( P < 0.05) as shown by increased total [3H]TBOB binding. Finally, a comparative ex vivo measurement compared endogenous GABA levels and suggested a trend towards higher GABA concentrations in MGB than in IC. Collectively, these studies suggest that, per unit GABA, high affinity extrasynaptic and synaptic GABAARs confer a significant inhibitory GABAAR advantage to MGB neurons relative to IC neurons. This increased GABA sensitivity likely underpins the vital filtering role of auditory thalamus.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
James Alexander Taylor ◽  
Masashi Hasegawa ◽  
Chloé Maëlle Benoit ◽  
Joana Amorim Freire ◽  
Marine Theodore ◽  
...  

AbstractCortical and limbic brain areas are regarded as centres for learning. However, how thalamic sensory relays participate in plasticity upon associative learning, yet support stable long-term sensory coding remains unknown. Using a miniature microscope imaging approach, we monitor the activity of populations of auditory thalamus (medial geniculate body) neurons in freely moving mice upon fear conditioning. We find that single cells exhibit mixed selectivity and heterogeneous plasticity patterns to auditory and aversive stimuli upon learning, which is conserved in amygdala-projecting medial geniculate body neurons. Activity in auditory thalamus to amygdala-projecting neurons stabilizes single cell plasticity in the total medial geniculate body population and is necessary for fear memory consolidation. In contrast to individual cells, population level encoding of auditory stimuli remained stable across days. Our data identifies auditory thalamus as a site for complex neuronal plasticity in fear learning upstream of the amygdala that is in an ideal position to drive plasticity in cortical and limbic brain areas. These findings suggest that medial geniculate body’s role goes beyond a sole relay function by balancing experience-dependent, diverse single cell plasticity with consistent ensemble level representations of the sensory environment to support stable auditory perception with minimal affective bias.


2007 ◽  
Vol 98 (4) ◽  
pp. 1941-1952 ◽  
Author(s):  
Mark N. Wallace ◽  
Lucy A. Anderson ◽  
Alan R. Palmer

Accurate temporal coding of low-frequency tones by spikes that are locked to a particular phase of the sine wave (phase-locking), occurs among certain groups of neurons at various processing levels in the brain. Phase-locked responses have previously been studied in the inferior colliculus and neocortex of the guinea pig and we now describe the responses in the auditory thalamus. Recordings were made from 241 single units, 32 (13%) of which showed phase-locked responses. Units with phase-locked responses were mainly (82%) located in the ventral division of the medial geniculate body (MGB), and also the medial division (18%), but were not found in the dorsal or shell divisions. The upper limiting frequency of phase-locking varied greatly between units (60–1,100 Hz) and between anatomical divisions. The upper limit in the ventral division was 520 Hz and in the medial was 1,100 Hz. The range of steady-state delays calculated from phase plots also varied: ventral division, 8.6–14 ms (mean 11.1 ms; SD 1.56); medial division, 7.5–11 ms (mean 9.3 ms; SD 1.5). Taken together, these measurements are consistent with the medial division receiving a phase-locked input directly from the brain stem, without an obligatory relay in the inferior colliculus. Cells in both the ventral and medial divisions of the MGB showed a response that phase-locked to the fundamental frequency of a guinea pig purr and may be involved in analyzing communication calls.


2002 ◽  
Vol 88 (5) ◽  
pp. 2377-2386 ◽  
Author(s):  
Jufang He

on and off auditory responses were examined in the medial geniculate body (MGB) of the guinea pig. Single- and multiunit recordings were carried out on 12 anesthetized animals, and noise-burst or pure-tone stimuli were applied to the ear contralateral to the recording hemisphere. One hundred and thirty-fiveoff or on-off neurons and 160 onneurons were studied, and the tuning curves of 21 on-off oroff neurons were examined from various nuclei of the MGB. The mean minimum threshold of the off responses (40.8 ± 20.0 dB SPL, mean ± SD; range: 0–80 dB SPL) was significantly higher than that of the on responses (28.5 ± 17.6 dB SPL, range: 0–60 dB SPL; n = 17, P < 0.001). Of 10 on-off neurons that showed identifiable tuning frequencies for both on andoff responses, 7 showed a higher off thanon best frequency (BF), 2 showed the same BF for bothon and off, and only 1 showed a slightly loweroff than on BF. Most off responses sampled from the borders of the ventral (MGv) and the rostromedial (MGrm) nuclei of the MGB showed single-peaked tuning curves, similar to those of the on responses in the MGv. The neurons located in the shell (MGs) and dorsal (MGd) nuclei of the MGB showed complicated—either multi-peaked or broad—tuning curves. Alloff responses showed long-duration-selectivity for acoustic stimuli: the mean half-maximum duration was 116.5 ± 114.8 ms ( n = 19, range: 27–411 ms). The latencies of 135off responses were studied in various divisions of the MGB. The ventral border region of MGv showed the shortest latency, followed by the dorsal border region of the MGv, the MGrm, and the caudomedial nucleus (MGcm) of the MGB. The posterior nucleus of the thalamus (Po), the MGd, and the MGs showed much longer mean latencies of >30 ms ( P < 0.05 compared with the border regions of the MGv, ANOVA), with Po showing the greatest mean latency of 60.3 ms and the greatest deviation of 25.5 ms). The latency of the offresponse (29.0 ± 14.0 ms, n = 135) was significantly greater than that of the on response (15.6 ± 9.6 ms, n = 160, P < 0.001). The present results provide valuable information about the threshold, frequency tuning characteristics, minimal response latency, and duration selectivity of off neurons in the auditory thalamus.


2022 ◽  
Vol 15 ◽  
Author(s):  
Marcus Jeschke ◽  
Frank W. Ohl ◽  
Xiaoqin Wang

The auditory thalamus is the central nexus of bottom-up connections from the inferior colliculus and top-down connections from auditory cortical areas. While considerable efforts have been made to investigate feedforward processing of sounds in the auditory thalamus (medial geniculate body, MGB) of non-human primates, little is known about the role of corticofugal feedback in the MGB of awake non-human primates. Therefore, we developed a small, repositionable cooling probe to manipulate corticofugal feedback and studied neural responses in both auditory cortex and thalamus to sounds under conditions of normal and reduced cortical temperature. Cooling-induced increases in the width of extracellularly recorded spikes in auditory cortex were observed over the distance of several hundred micrometers away from the cooling probe. Cortical neurons displayed reduction in both spontaneous and stimulus driven firing rates with decreased cortical temperatures. In thalamus, cortical cooling led to increased spontaneous firing and either increased or decreased stimulus driven activity. Furthermore, response tuning to modulation frequencies of temporally modulated sounds and spatial tuning to sound source location could be altered (increased or decreased) by cortical cooling. Specifically, best modulation frequencies of individual MGB neurons could shift either toward higher or lower frequencies based on the vector strength or the firing rate. The tuning of MGB neurons for spatial location could both sharpen or widen. Elevation preference could shift toward higher or lower elevations and azimuth tuning could move toward ipsilateral or contralateral locations. Such bidirectional changes were observed in many parameters which suggests that the auditory thalamus acts as a filter that could be adjusted according to behaviorally driven signals from auditory cortex. Future work will have to delineate the circuit elements responsible for the observed effects.


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