Local field potentials from different visual cortical areas and subdivisions of the cat's lateral posterior-pulvinar complex of the thalamus (LP-P) were recorded during a behavioral task based on delayed spatial discrimination of visual or auditory stimuli. During visual but not auditory attentive tasks, we observed an increase of beta activity (12-25 Hz) as calculated from signals recorded from the caudal part of the lateral zone of the LP-P (LPl-c) as well as from cortical areas 17 and 18 and the complex located at the middle suprasylvian sulcus (MSS). This beta activity appeared only in the trials that ended with a successful response, proving its relationship to the mechanism of visual attention. In contrast, no enhanced beta activity was observed in the rostral part of the lateral zone of the LP-P and in the pulvinar proper. Two subregions of LPl-c (ventromedial and dorsolateral) were distinguished by visually related, attentional beta activity of low (12-18 Hz) and high (18-25 Hz) frequencies, respectively. At the same time, area 17 exhibited attentional activation in the whole beta range, and an increase of power in low-frequency beta was observed in the medial bank of MSS, whereas cortical area 18 and the lateral bank of the MSS were activated in the high beta range. Phase-correlation analysis revealed that two distinct corticothalamic systems were synchronized by the beta activity of different frequencies. One comprised of cortical area 17, ventromedial region of LPl-c, and medial MSS, the second involved area 18 and the dorsolateral LPl-c. Our observations suggest that LPl-c belongs to the wide corticothalamic attentional system, which is functionally segregated by distinct streams of beta activity.

https://www.jneurosci.org/content/jneuro/27/9/2230.full.pdf

Two Streams of Attention-Dependent β Activity in the Striate Recipient Zone of Cat's Lateral Posterior–Pulvinar Complex

To provide a quantitative comparison of the synaptic organization of "first-order" and "higher-order" thalamic nuclei, we followed bias-corrected sampling methods identical to a previous study of the cat dorsal lateral geniculate nucleus (dLGN; Van Horn et al. [2000] J. Comp. Neurol. 416:509-520) to examine the distribution of terminal types within the cat pulvinar nucleus. We observed the following distribution of synaptic contacts: large terminals that contain loosely packed round vesicles (RL profiles), 3.5%; presynaptic profiles that contain densely packed pleomorphic vesicles (F1 profiles), 7.3%; profiles that could be both presynaptic and postsynaptic that contain loosely packed pleomorphic vesicles (F2 profiles), 5.0%; and small terminals that contain densely packed round vesicles (RS profiles), 84.2%. Postembedding immunocytochemistry for gamma-aminobutyric acid (GABA) was used to distinguish the postsynaptic targets as thalamocortical cells or interneurons. The distribution of synaptic contacts on thalamocortical cells was as follows: RL profiles, 2.1%; F1 profiles, 6.9%; F2 profiles, 5.4%; and RS profiles, 85.6%. The distribution of synaptic contacts on interneurons was as follows: RL profiles, 11.8%; F1 profiles, 9.7%; F2 profiles, 2.8%; and RS profiles, 75.6%. These distributions are similar to that found within the dLGN in that the RS inputs (the presumed "modulators") far outnumber the RL inputs (the presumed "drivers"). However, in comparison to the dLGN, the pulvinar nucleus receives significantly fewer numbers of RL, F1, and F2 contacts and significantly higher numbers of RS contacts. Thus, the RS/RL synapse ratio in the pulvinar nucleus is 24:1, in contrast to the 5:1 RS/RL synapse ratio in the dLGN (Van Horn et al., 2000). In first-order nuclei, the lower RS/RL synapse ratio may result in the transfer of visual information that is largely unmodified. In contrast, in higher-order nuclei, the higher RS/RL synapse ratio may allow for a finer modulation of driving inputs.

Relative distribution of synapses in the pulvinar nucleus of the cat: implications regarding the "driver/modulator" theory of thalamic function.

Thalamic nuclei have long been considered as passive relay stations for sensory signals en route to the cerebral cortex, where higher level processing occurs. In recent years, it has been proposed that thalamic nuclei may actively participate in the processing of specific information in conjunction with cortical areas. In support of this hypothesis, we recently discovered that neurons in the main extrageniculate visual nucleus, the pulvinar, exhibit higher-order visual properties that were, until now, only associated with higher-order cortical areas. Pulvinar neurons can indeed code the veridical direction of a moving plaid pattern, indicating that these cells can integrate ambiguous signals into a coherent percept. This finding as well as our demonstration that there are cortico-thalamo-cortical loops involved in complex motion analysis open promising avenues in unraveling the function of the pulvinar complex in normal vision.

Chapter 5 Higher-order motion processing in the pulvinar

Huppe-Gourgues F, Bickford ME, Boire D, Ptito M, Casanova C. The lateral posterior (LP) nucleus is a higher order thalamic nucleus that is believed to play a key role in the transmission of visual information between cortical areas. Two types of cortical terminals have been identified in higher order nuclei, large (type II) and smaller (type I), which have been proposed to drive and modulate, respectively, the response properties of thalamic cells (Sherman and Guillery [1998] Proc. Natl. (...)

Distribution, morphology, and synaptic targets of corticothalamic terminals in the cat lateral posterior‐pulvinar complex that originate from the posteromedial lateral suprasylvian cortex

Spatial and temporal visual properties of single neurons in the suprageniculate nucleus of the thalamus.

The cat's lateral posterior-pulvinar complex (LP-pulvinar) contains three main representations of the visual field. The lateral part of the LP nucleus (LPl or striate-recipient zone) is the only region of these extrageniculate nuclei which receives afferents from the primary visual cortex. We investigated the contribution of area 17 to the response properties (orientation and spatial frequency tuning functions) of LPl neurons by cooling or lesioning the visual cortex. Responses of 40 LPl cells were studied before, during and after the reversible cooling of the striate cortex. When tested for orientation, a total of 10 units out of 28 was affected (36%). For most of these cells (eight of 10), cooling the visual cortex yielded a reduction of the cells' visual responses without altering their orientation-selectivity (there was no significant change in the orientation tuning width). For only two cells, inactivation led to an increase in the response amplitude. Also, blocking the visual cortex never modified the direction-selectivity of LPl cells. When tested for spatial frequency, 12 neurons out of 33 were affected (36%) by the experimental protocol. In most cases, we observed a reduction in the responses at each spatial frequency tested, with no change in tuning bandwidth. For only three LPl cells, the effects of inactivation of the visual cortex were restricted to specific spatial frequencies, altering the profile of the spatial frequency tuning function. In five cats, removing area 17 reduced the proportion of visual neurons in LPl and the spared visually evoked responses were noticeably depressed. Despite the reduction in responsiveness, a few LPl receptive fields within the cortical scotoma were still sensitive to the orientation and/or direction of a moving stimulus. This last observation suggests that some properties in LPl could be generated either by circuits intrinsic to the LPl or by afferents from extrastriate cortical areas. Overall, these results indicate that projections from the visual cortex to the striate-recipient zone of the LP-pulvinar complex are mainly excitatory. Despite the strong impact of the area 17 projections, our data suggest that the extrastriate cortex could also play a role in the establishment of response properties in the cat's LPl.

S Darveau

Papers

Contribution of Area 17 to Cell Responses in the Striate‐recipient Zone of the Cat's Lateral Posterior‐Pulvinar Complex