Amblyopia decreases activation of the corticogeniculate pathway and visualthalamic reticularis in attentive rats: A 'focal attention' hypothesis

In rats which were rendered monocular amblyopic by lid suturing one eye dur ing a critical period, the intensity of neuronal activation in parts of the monocular segments of the striate cortex (layers 4 and 6) and lateral geni culate nucleus, and in the visual segment of the thalamic reticular nucleus , was determined after exploration of a novel-complex environment. Quantita tive analysis of the number of Fos-labelled neurons per unit area showed th at, in comparison to the structures contralateral to the normal eye, in the side contralateral to the deprived amblyopic eye there is a gradient of di minished 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 lat eral geniculate there was no Fos-detectable activation asymmetry. Furthermo re, there was a positive correlation between the time rats spent in explora tion 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 predomi nantly under visual cortical control via the cortico-reticulo-geniculate pa thway originating in layer 6, because this layer showed activation asymmetr y 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 correlate d to the amount of exploratory attentional behaviour. (3) Diminished activi ty in the cortico-reticulo-geniculate pathway originating in layer 6, and o f visual reticularis, caused by visual deprivation during the critical peri od 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 vis ual reticularis in exploring animals is necessarily a reflection of activat ion of the corticogeniculate pathway, because these axons innervate both th e geniculate and the visual reticular segment. Mechanistically, a focus of animal's attention is transmitted in a top-down fashion from the extrastria te cortex, and from upper cortical layers, into striate cortex layer 6. In turn, activation of layer 6 cells corresponding to attentional foci generat es a core of excitation in the geniculate by the direct glutamatergic corti cogeniculate axons, and a surround inhibition by the disynaptic cortico-ret iculo-geniculate (ultimately GABAergic) pathway. In the temporal domain, in light of recent results, activation of thalamic reticular nucleus visual s egment will contribute to the induction of gamma oscillations in geniculoco rtical pathways and in their cortical targets. All together, these interactions result in increased effectiveness of thala mocortical transmission of features from the focalized visual scene. The po stulated attention-dependent spatiotemporal influences on thalamocortical t ransmission would be a main function of the corticothalamic pathways in the awake, attentive animal. (C) 1999 IBRO. published by Elsevier Science Ltd.