Diverse subthreshold cross‐modal sensory interactions in the thalamic reticular nucleus: implications for new pathways of cross‐modal attentional gating function

Our attention to a sensory cue of a given modality interferes with attention to a sensory cue of another modality. However, an object emitting various sensory cues attracts attention more effectively. The thalamic reticular nucleus (TRN) could play a pivotal role in such cross‐modal modulation of attention given that cross‐modal sensory interaction takes place in the TRN, because the TRN occupies a highly strategic position to function in the control of gain and/or gating of sensory processing in the thalamocortical loop. In the present study cross‐modal interactions between visual and auditory inputs were examined in single TRN cells of anesthetised rats using juxta‐cellular recording and labeling techniques. Visual or auditory responses were modulated by subthreshold sound or light stimuli, respectively, in the majority of recordings (46 of 54 visual and 60 of 73 auditory cells). However, few bimodal sensory cells were found. Cells showing modulation of the sensory response were distributed in the whole visual and auditory sectors of the TRN. Modulated cells sent axonal projections to first‐order or higher‐order thalamic nuclei. Suppression predominated in modulation that took place not only in primary responses but also in late responses repeatedly evoked after sensory stimulation. Combined sensory stimulation also evoked de‐novo responses, and modulated response latency and burst spiking. These results indicate that the TRN incorporates sensory inputs of different modalities into single cell activity to function in sensory processing in the lemniscal and non‐lemniscal systems. This raises the possibility that the TRN constitutes neural pathways involved in cross‐modal attentional gating.     

Axonal projections of auditory cells with short and long response latencies in the medial geniculate nucleus: distinct topographies in the connection with the thalamic reticular nucleus

The thalamic reticular nucleus (TRN) is a crucial anatomical node of thalamocortical connectivity for sensory processing. In the rat auditory system, we determined features of thalamic projections to the TRN, using juxtacellular recording and labeling techniques. Two types of auditory cells (short latency, SL, and long latency, LL), exhibiting unit discharges to noise burst stimuli (duration, 100 ms) with short (< 50 ms) and long (> 100 ms) response latencies, were obtained from the ventral division of the medial geniculate nucleus (MGV). Both SL and LL cells had a propensity to exhibit reverberatory discharges in response to sound stimuli. The primary discharges of SL cells were mostly single spikes while the non-primary discharges of SL cells and the whole discharges of LL cells were mostly burst spikes. SL cells sent topographic projections to the TRN along the dorsoventral and rostrocaudal neural axes while LL cells only along the rostrocaudal axis. As tonotopy-related cortical projections to the TRN are topographic primarily along the dorsoventral extent of the TRN and the MGV is tonotopically organized along the dorsoventral axis, SL cells, directly activated by ascending auditory inputs, may be closely involved in tonotopic thalamocortical connectivity. On the other hand, LL cells, which are suppressed by ascending inputs and could be driven to discharge by corticofugal inputs, are assumed to activate the TRN in a manner less related to tonotopic organization. There may exist heterogeneous projections from the MGV to the TRN, which, in conjunction with corticofugal connections, could constitute distinct channels of auditory processing.     

Axonal projections of single auditory neurons in the thalamic reticular nucleus: implications for tonotopy-related gating function and cross-modal modulation

Tonotopically comparable subfields of the primary auditory area (AI) and nonprimary auditory areas (non-AI), i.e. posterodorsal area (PD) and ventral auditory area (VA), in the rat cortex have similar topographies in the projection to the ventral division of the medial geniculate nucleus (MGV), but reverse topographies in the projection to the thalamic reticular nucleus (TRN). In this study, we examined axonal projections of single auditory TRN cells, using juxtacellular recording and labeling techniques, to determine features of TRN projections and estimate how the TRN mediates corticofugal inhibition along with the reverse topographies of cortical projections to the TRN. Auditory TRN cells sent topographic projections to limited parts of the MGV in a manner that relays cortical inputs from tonotopically comparable subfields of the AI and non-AI (PD and VA) to different parts of the MGV. The results suggest that corticofugal excitations from the AI and non-AI modulate thalamic cell activity in the same part of the MGV, whereas corticofugal inhibitions via the TRN modulate cell activity in different parts of the MGV with regard to tonotopic organization. The AI and non-AI could serve distinctive gating functions for auditory attention through the differential topography of inhibitory modulation. In addition, we obtained an intriguing finding that a subset of auditory TRN cells projected to the somatosensory but not to the auditory thalamic nuclei. There was also a cell projecting to the MGV and somatosensory nuclei. These findings extend the previously suggested possibility that TRN has a cross-modal as well as an intramodal gating function in the thalamus.     

Auditory thalamic reticular nucleus of the rat: anatomical nodes for modulation of auditory and cross-modal sensory processing in the loop connectivity between the cortex and thalamus

The auditory sector of the thalamic reticular nucleus (TRN) plays a pivotal role in gain and/or gate control of auditory input relayed from the thalamus to cortex. The TRN is also likely involved in cross-modal sensory processing for attentional gating function. In the present study, we anatomically examined how cortical and thalamic afferents intersect in the auditory TRN with regard to these two functional pathways. Iontophoretic injections of biocytin into subregions of the auditory TRN, which were made with the guidance of electrophysiological recording of auditory response, resulted in retrograde labeling of cortical and thalamic cells, indicating the sources of afferents to the TRN. Cortical afferents from area Te1 (temporal cortex, area 1), which contains the primary and anterior auditory fields, topographically intersected thalamic afferents from the ventral division of the medial geniculate nucleus at the subregions of the auditory TRN, suggesting tonotopically organized convergence of afferents, although they innervated a given small part of the TRN from large parts. In the caudodorsal and rostroventral parts of the auditory TRN, cortical afferents from nonprimary visual and somatosensory areas intersected thalamic afferents from auditory, visual, and somatosensory nuclei. Furthermore, afferents from the caudal insular cortex and the parvicellular part of the ventral posterior thalamic nucleus, which are associated with visceral processing, converged to the rostroventral end of the auditory TRN. The results suggest that the auditory TRN consists of anatomical nodes that mediate tonotopic and/or cross-modal modulation of auditory and other sensory processing in the loop connectivity between the cortex and thalamus.     

Variations on the theme of musical expertise: cognitive and sensory processing in percussionists,vocalists and non‐musicians

Comparisons of musicians and non‐musicians have revealed enhanced cognitive and sensory processing in musicians, with longitudinal studies suggesting these enhancements may be due in part to experience‐based plasticity. Here, we investigate the impact of primary instrument on the musician signature of expertise by assessing three groups of young adults: percussionists, vocalists, and non‐musician controls. We hypothesize that primary instrument engenders selective enhancements reflecting the most salient acoustic features to that instrument, whereas cognitive functions are enhanced regardless of instrument. Consistent with our hypotheses, percussionists show more precise encoding of the fast‐changing acoustic features of speech than non‐musicians, whereas vocalists have better frequency discrimination and show stronger encoding of speech harmonics than non‐musicians. There were no strong advantages to specialization in sight‐reading vs. improvisation. These effects represent subtle nuances to the signature since the musician groups do not differ from each other in these measures. Interestingly, percussionists outperform both non‐musicians and vocalists in inhibitory control. Follow‐up analyses reveal that within the vocalists and non‐musicians, better proficiency on an instrument other than voice is correlated with better inhibitory control. Taken together, these outcomes suggest the more extensive engagement of motor systems during instrumental practice may be an important factor for enhancements in inhibitory control, consistent with evidence for overlapping neural circuitry involved in both motor and cognitive control. These findings contribute to the ongoing refinement of the musician signature of expertise and may help to inform the use of music in training and intervention to strengthen cognitive function.     

The hyperpolarization‐activated non‐specific cation current (Ih) adjusts the membrane properties,excitability, and activity pattern of the giant cells in the rat dorsal cochlear nucleus

Giant cells of the cochlear nucleus are thought to integrate multimodal sensory inputs and participate in monaural sound source localization. Our aim was to explore the significance of a hyperpolarization‐activated current in determining the activity of giant neurones in slices prepared from 10 to 14‐day‐old rats. When subjected to hyperpolarizing stimuli, giant cells produced a 4‐(N‐ethyl‐N‐phenylamino)‐1,2‐dimethyl‐6‐(methylamino) pyridinium chloride (ZD7288)‐sensitive inward current with a reversal potential and half‐activation voltage of –36 and –88 mV, respectively. Consequently, the current was identified as the hyperpolarization‐activated non‐specific cationic current (I_h). At the resting membrane potential, 3.5% of the maximum I_h conductance was available. Immunohistochemistry experiments suggested that hyperpolarization‐activated, cyclic nucleotide‐gated, cation non‐selective (HCN)1, HCN2, and HCN4 subunits contribute to the assembly of the functional channels. Inhibition of I_h hyperpolarized the membrane by 6 mV and impeded spontaneous firing. The frequencies of spontaneous inhibitory and excitatory postsynaptic currents reaching the giant cell bodies were reduced but no significant change was observed when evoked postsynaptic currents were recorded. Giant cells are affected by biphasic postsynaptic currents consisting of an excitatory and a subsequent inhibitory component. Inhibition of I_h reduced the frequency of these biphasic events by 65% and increased the decay time constants of the inhibitory component. We conclude that I_h adjusts the resting membrane potential, contributes to spontaneous action potential firing, and may participate in the dendritic integration of the synaptic inputs of the giant neurones. Because its amplitude was higher in young than in adult rats, I_h of the giant cells may be especially important during the postnatal maturation of the auditory system.