Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a `focal attention' hypothesis

Abstract

In rats which were rendered monocular amblyopic by lid suturing one eye during a critical period, the intensity of neuronal activation in parts of the monocular segments of the striate cortex (layers 4 and 6) and lateral geniculate nucleus, and in the visual segment of the thalamic reticular nucleus, was determined after exploration of a novel-complex environment. Quantitative analysis of the number of Fos-labelled neurons per unit area showed that, in comparison to the structures contralateral to the normal eye, in the side contralateral to the deprived amblyopic eye there is a gradient of diminished activation. The strongest activation asymmetry was observed in the visual reticular segment, while in layers 6 and 4 of the visual cortex the activation asymmetry was less strong and weakest, respectively. In the lateral geniculate there was no Fos-detectable activation asymmetry. Furthermore, there was a positive correlation between the time rats spent in exploration and the degree of activation asymmetry in the visual reticular segment. From these results it is concluded: (1) Activation of the visual segment of the thalamic reticular nucleus in the alert, attentive animal is predominantly under visual cortical control via the cortico-reticulo-geniculate pathway originating in layer 6, because this layer showed activation asymmetry while the other visual input to reticularis, the geniculate, did not show this asymmetry. (2) Activation of the visual reticularis is a function of attention to the environment because its activation asymmetry was correlated to the amount of exploratory attentional behaviour. (3) Diminished activity in the cortico-reticulo-geniculate pathway originating in layer 6, and of visual reticularis, caused by visual deprivation during the critical period should be considered as additional etiological factors of the resulting amblyopia. The functional significance of these results is explained by a `focal attention' hypothesis postulating that the observed activation of visual reticularis in exploring animals is necessarily a reflection of activation of the corticogeniculate pathway, because these axons innervate both the geniculate and the visual reticular segment. Mechanistically, a focus of animal's attention is transmitted in a top-down fashion from the extrastriate cortex, and from upper cortical layers, into striate cortex layer 6. In turn, activation of layer 6 cells corresponding to attentional foci generates a core of excitation in the geniculate by the direct glutamatergic corticogeniculate axons, and a surround inhibition by the disynaptic cortico–reticulo–geniculate (ultimately GABAergic) pathway. In the temporal domain, in light of recent results, activation of thalamic reticular nucleus visual segment will contribute to the induction of gamma oscillations in geniculocortical pathways and in their cortical targets. All together, these interactions result in increased effectiveness of thalamocortical transmission of features from the focalized visual scene. The postulated attention-dependent spatiotemporal influences on thalamocortical transmission would be a main function of the corticothalamic pathways in the awake, attentive animal.