Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning

McAlonan, Kerry; Brown, Verity J.; Bowman, Eric

doi:10.1523/jneurosci.20-23-08897.2000

Cited by 113 publications

(58 citation statements)

References 31 publications

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“…In monkey and rodent, shifting the animal's attention from one sensory modality to another increased the neuronal activity in the TRN sector associated with the attended stimulus (McAlonan et al 2000(McAlonan et al , 2006. Conversely, during an attentional task involving valid and invalid cues, unilateral TRN lesions abolished the processing advantage conferred by cues contralateral to the lesion (Weese et al 1999).…”

Section: Functional Implicationsmentioning

confidence: 97%

Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Cotillon-Williams¹,

Huetz²,

Hennevin³

et al. 2008

Journal of Neurophysiology

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Cotillon-Williams N, Huetz C, Hennevin E, Edeline J-M. Tonotopic control of auditory thalamus frequency tuning by reticular thalamic neurons. J Neurophysiol 99: 1137-1151, 2008. First published December 26, 2007 doi:10.1152/jn.01159.2007. GABAergic cells of the thalamic reticular nucleus (TRN) can potentially exert strong control over transmission of information through thalamus to the cerebral cortex. Anatomical studies have shown that the reticulothalamic connections are spatially organized in the visual, somatosensory, and auditory systems. However, the issue of how inhibitory input from TRN controls the functional properties of thalamic relay cells and whether this control follows topographic rules remains largely unknown. Here we assessed the consequences of increasing or decreasing the activity of small ensembles of TRN neurons on the receptive field properties of medial geniculate (MG) neurons. For each MG cell, the frequency tuning curve and the rate-level function were tested before, during, and after microiontophoretic applications of GABA, or of glutamate, in the auditory sector of the TRN. For 66 MG cells tested during potent pharmacological control of TRN activity, group data did not reveal any significant effects. However, for a population of 20/66 cells (all but 1 recorded in the ventral, tonotopic, division), the breadth of tuning, the frequency selectivity and the acoustic threshold were significantly modified in the directions expected from removing, or reinforcing, a dominant inhibitory input onto MG cells. Such effects occurred only when the distance between the characteristic frequency of the recorded ventral MG cell and that of the TRN cells at the ejection site was Ͻ0.25 octaves; they never occurred for larger distances. This relationship indicates that the functional interactions between TRN cells and ventral MG cells rely on precise topographic connections. I N T R O D U C T I O NThe thalamus is often considered as a "gate" for the transfer of information to neocortex. Understanding the key factors controlling this gate has been the subject of intense research, but several points remain unresolved. The reticular nucleus of the thalamus (TRN) has a key anatomical position and chemical composition to modulate thalamocortical activity. It receives inputs from both thalamus and cortex and sends outputs back to the thalamus (Jones 1975). Exclusively composed of GABAergic neurons (Arcelli et al. 1997; Benson et al. 1991;Houser et al. 1980), it is a major source of inhibition for all thalamic nuclei . In some species and for some sensory modalities, it is the quasi-exclusive source of inhibition in the thalamus, whereas in others it shares this role with local inhibitory interneurons (reviewed in Jones 1985; Sherman and Guillery 2001). The lateral geniculate nucleus possesses around 20% of inhibitory interneurons in all species (Barbaresi et al. 1986; Benson et al. 1992). The somatosensory thalamus and the auditory thalamus possess 20 -25% of inhibitory interneurons in primate and cat (Benson e...

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Section: Functional Implicationsmentioning

confidence: 97%

Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Cotillon-Williams¹,

Huetz²,

Hennevin³

et al. 2008

Journal of Neurophysiology

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“…In most sensory systems, the majority of feedback passes through the thalamus, which has been suggested to act as an "attentional gate" (McAlonan et al 2000;Spence et al 2001). Olfactory information, however, does not pass through the thalamus as it projects to higher cortical regions; because of this, some researchers have suggested that attentional processes cannot be applied to olfactory stimuli as to other stimuli (Smythies 1997).…”

Section: Centrifugal Projections In Olfactionmentioning

confidence: 99%

Role of centrifugal projections to the olfactory bulb in olfactory processing

Kiselycznyk

Zhang²,

Linster³

2006

Learn. Mem.

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While there is evidence that feedback projections from cortical and neuromodulatory structures to the olfactory bulb are crucial for maintaining the oscillatory dynamics of olfactory bulb processing, it is not clear how changes in dynamics are related to odor perception. Using electrical lesions of the olfactory peduncle, sparing output from the olfactory bulb while decreasing feedback inputs to the olfactory bulb, we demonstrate here a role for feedback inputs to the olfactory bulb in the formation of odor–reward associations, but not for maintaining primary bulbar odor representations, as reflected by spontaneous odor discrimination.

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“…Lesions of visual TRN abolished priming effects associated with cues to contralateral visual targets in an attentional orienting task (Weese et al, 1999), demonstrating a link between TRN and the attentional effects of visual cues. Other studies focused on the interactions between the modality-specific sectors of TRN, showing a selective increase in Fos-positive neurons in the sector of TRN associated with the modality of the attended stimulus (Montero, 1997(Montero, , 1999(Montero, , 2000McAlonan et al, 2000). Although these lesion and histological studies provide evidence that modulation of TRN occurs with attention, they could not address whether the changes were increases or decreases of activity or whether the changes occurred fast enough to modulate visual responses in the LGN.…”

Section: Introductionmentioning

confidence: 98%

Attentional Modulation of Thalamic Reticular Neurons

McAlonan

Cavanaugh²,

Wurtz³

2006

J. Neurosci.

231

156

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The major pathway for visual information reaching cerebral cortex is through the lateral geniculate nucleus (LGN) of the thalamus. Acting on this vital relay is another thalamic nucleus, the thalamic reticular nucleus (TRN). This nucleus receives topographically organized collaterals from both thalamus and cortex and sends similarly organized projections back to thalamus. The inputs to the TRN are excitatory, but the output back to the thalamic relay is inhibitory, providing an ideal organization for modulating visual activity during early processing. This functional architecture led Crick in 1984 to hypothesize that TRN serves to direct a searchlight of attention to different regions of the topographic map; however, despite the substantial influence of this hypothesis, the activity of TRN neurons has never been determined during an attention task. We have determined the nature of the response of visual TRN neurons in awake monkeys, and the modulation of that response as the monkeys shifted attention between visual and auditory stimuli. Visual TRN neurons had a strong (194 spikes/s) and fast (25 ms latency) transient increase of activity to spots of light falling in their receptive fields, as well as high background firing rate (45 spikes/s). When attention shifted to the spots of light, the amplitude of the transient visual response typically increased, whereas other neuronal response characteristics remained unchanged. Thus, as predicted previously, TRN activity is modified by shifts of visual attention, and these attentional changes could influence visual processing in LGN via the inhibitory connections back to the thalamus.

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Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning

Cited by 113 publications

References 31 publications

Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Tonotopic Control of Auditory Thalamus Frequency Tuning by Reticular Thalamic Neurons

Role of centrifugal projections to the olfactory bulb in olfactory processing

Attentional Modulation of Thalamic Reticular Neurons

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