Scientific Understanding of Consciousness
Attention Regulated by Thalamocortical Activity between Pulvinar and Cortex
Science 10 August 2012: Vol. 337 no. 6095 pp. 753-756
The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands
Yuri B. Saalmann, Mark A. Pinsk, Liang Wang, Xin Li, Sabine Kastner
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544, USA.
2Department of Psychology, Princeton University, Princeton, NJ 08544, USA.
Selective attention mechanisms route behaviorally relevant information through large-scale cortical networks. Although evidence suggests that populations of cortical neurons synchronize their activity to preferentially transmit information about attentional priorities, it is unclear how cortical synchrony across a network is accomplished. Based on its anatomical connectivity with the cortex, we hypothesized that the pulvinar, a thalamic nucleus, regulates cortical synchrony. We mapped pulvino-cortical networks within the visual system, using diffusion tensor imaging, and simultaneously recorded spikes and field potentials from these interconnected network sites in monkeys performing a visuospatial attention task. The pulvinar synchronized activity between interconnected cortical areas according to attentional allocation, suggesting a critical role for the thalamus not only in attentional selection but more generally in regulating information transmission across the visual cortex.
The limited capacity of the visual system does not permit simultaneous processing of all information from our cluttered environment in detail. Selective attention helps overcome this limitation by preferentially routing behaviorally relevant information across the visual system. Simultaneous neural recordings from two cortical areas have suggested that this selective routing depends on the degree of synchrony between neuronal groups in each cortical area. However, it is unclear how different cortical areas synchronize their activity. Although direct interaction between two cortical areas may give rise to their synchrony, an alternative possibility is that a third area, connected to both of them, mediates cortical synchronization.
Higher-order thalamic nuclei, such as the pulvinar, predominantly receive input from the cortex rather than the periphery, and their output strongly influences cortical activity in in vitro experiments. Because directly connected cortical areas are also indirectly connected via the pulvinar, the pulvinar is ideally positioned to synchronize activity across the visual cortex. However, little is known about the functional role of these cortico-pulvino-cortical loops. Selective attention modulates the magnitude of response of macaque pulvinar neurons, and both humans and macaques with pulvinar lesions commonly have attentional deficits. We therefore hypothesized that the pulvinar increases synchrony between sequential processing stages across the visual cortex during selective attention.
Information transmitted along the ventral visual cortical pathway is sequentially processed in interconnected areas V4 and the temporo-occipital area (TEO). We simultaneously recorded neural activity in macaques in the pulvinar, V4, and TEO during 51 recording sessions. Spike trains and local field potentials (LFPs) were recorded in each area from neurons with overlapping receptive fields (RFs). Monkeys performed a variant of the Eriksen flanker task, in which a spatial cue signals the location of a subsequent target flanked by distracter stimuli (target detection >80% accuracy overall. Because directly connected cortical areas such as V4 and TEO only connect with restricted but overlapping zones in the pulvinar, we used diffusion tensor imaging (DTI) to ensure that electrodes targeted interconnected pulvino-cortical sites.
We performed probabilistic tractography on DTI data for each monkey to map probable connections between the pulvinar, V4, and TEO.
We further tested whether attention influenced pulvinar spike timing, specifically the synchrony between pulvinar neurons, by calculating the degree of synchrony between spike times and the LFP, or spike-field coherence.
Pulvinar spike-field coherence increased immediately after the cue appeared in the RF, predominantly in the alpha-frequency range.
We next aimed to establish that selective attention increased synchrony between cortical areas. We calculated the coherence between V4 and TEO LFPs, which measures the synchrony between oscillatory processes in the two areas, as a function of oscillation frequency. Attention generally increased coherence between V4 and TEO LFPs in two frequency bands. There was significantly increased mean coherence in the 8- to 15-Hz range, as well as a smaller but significant increase in the 30- to 60-Hz range (gamma band) across the population.
Because low-frequency oscillations modulate higher-frequency oscillations, we tested whether attention increased cross-frequency coupling between alpha and gamma oscillations within V4 and TEO. To measure cross-frequency coupling, we calculated the synchronization index between cortical alpha oscillations and the gamma power envelope. Across the population, there was a significantly greater synchronization index for V4 and TEO during the delay period, when attention was directed to the RF location rather than outside the RF (sign tests, P < 0.05), suggesting that alpha oscillations contributed to the attention effect on gamma frequencies.
If the pulvinar interacts with the cortex during attentional processing, then attention should also modulate pulvino-cortical synchrony. Across the population, there was significantly greater alpha-band coherence between the pulvinar LFP and V4 LFP, as well as between the pulvinar LFP and TEO LFP during the delay period until target presentation, when the monkey attended to the RF location rather than outside the RF. Across the population, spatial attention significantly increased the coherence between pulvinar spikes and V4 LFP, as well as between pulvinar spikes and TEO LFP, predominantly in the 8- to 15-Hz range, throughout the delay period until target presentation (Holm’s controlled t tests, P < 0.05). These findings support the idea that the pulvinar is part of the brain’s attention network and that it uses the alpha band as a fundamental operating mode.
To determine the direction of pulvino-cortical interactions, we calculated the conditional Granger causality in the frequency domain for the connections between the pulvinar, V4, and TEO. Conditional Granger causality measures the influence that one area (e.g., the pulvinar) has on a second area (e.g., TEO), accounting for the influence of other areas (e.g., V4).
Pulvinar influence on alpha activity in both V4 and TEO correlated with the attentional modulation of synchrony between V4 and TEO in the same frequency range, suggesting that the pulvinar regulated alpha synchrony between cortical areas according to attention allocation.
Our results show that the pulvinar modulates the synchrony between cortical areas according to the locus of attention. The pulvinar predominantly influenced cortical alpha oscillations, consistent with another thalamic nucleus, the lateral geniculate nucleus, driving occipital alpha rhythms (25). Evidence suggests that the rhythmic excitability of alpha oscillations gates visual events, with the phase of alpha oscillations being critical for the transmission of visual information. Thus, the pulvinar, by synchronizing distributed patches of cortical alpha activity, can selectively facilitate transmission of information about attentional priorities across the cortex. Because pulvinar-controlled alpha activity modulated gamma activity in the cortex through cross-frequency coupling, pulvinar influence on cortical synchrony extends to frequencies higher than the alpha frequency.
Pulvinar control of cortical processing challenges the common conceptualizing of cognitive functions as being restricted to the cortex. Pulvino-cortical influences dominated during the delay period, suggesting that internal processes such as the maintenance of attention in expectation of visual stimuli and short-term memory rely heavily on pulvino-cortical interactions. Pulvinar regulation of alpha activity is consistent with the important role ascribed to alpha oscillations in these internal processes.
The prevailing view that information about our visual environment is transmitted through a network of cortical areas for detailed processing needs to be revised by considering extensive pulvino-cortical loops that regulate the information transmitted between each cortical stage of visual processing. Because of common cellular mechanisms and thalamo-cortical connectivity principles across sensorimotor domains, a general function of higher-order thalamic nuclei may be the regulation of cortical synchrony to selectively route information across the cortex.
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