Elsevier

Biosystems

Volume 89, Issues 1–3, May–June 2007, Pages 227-235
Biosystems

A hypothetical role of cortico-basal ganglia-thalamocortical loops in visual processing

https://doi.org/10.1016/j.biosystems.2006.04.020Get rights and content

Abstract

The goal of the present work was to define the mechanisms underlying the contribution of sensory and limbic cortico-basal ganglia-thalamocortical loops to visual processing and its attentional modulation. We proposed that visual processing is promoted by dopamine-dependent long-term modifications of synaptic transmission in the basal ganglia that favour a selection of neocortical patterns representing a visual stimulus. This selection is the result of the opposite sign of modulation of strong and weak cortico-basal ganglia inputs and subsequent activity reorganization in each loop. Reorganization leads to disinhibition/inhibition of cortical neurons strongly/weakly excited by stimulus during dopamine release. Recruitment of the thalamo-basal ganglia-collicular pathway is proposed to be necessary for stimulus-evoked dopamine release that underlies bottom-up attentional effects. Visual excitation of the prefrontal cortex and hippocampus (via the thalamus), their cooperation in control of the basal ganglia and dopaminergic cell firing, and simultaneous modulation of activity in diverse cortico-basal ganglia-thalamocortical loops is proposed to underlie top-down attentional effects. It follows from our model that only those components of cortical responses can be modulated by attention, whose onset exceeds the latency of visual responses of dopaminergic cells (50–110 ms). This and other consequences of the model are in accordance with known experimental data.

Introduction

Visual processing as well as other cognitive and attentional brain functions are supported by a number of parallel functionally segregated cortico-subcortical circuits involving the basal ganglia (BG) (Brown et al., 1997). The BG nuclei are part of topographically closed cortico-BG-thalamocortical (C-BG-Th-C) loops, since the targeted cortical area (visual or prefrontal) is both a target of the BG output and a source of input to the BG (Middleton and Strick, 1996, Middleton and Strick, 2002) (Fig. 1a). Input BG nucleus (dorsal striatum or ventral striatum (nucleus accumbens, NAcc)) is connected with output BG nucleus (substantia nigra pars reticulata (SNr)) via direct and indirect pathways, arising from GABAergic striatonigral (SN) and striatopallidal (SP) spiny cells, respectively (Alexander and Crutcher, 1990) (Fig. 1a). Cortical signals passing along the direct and indirect pathways disinhibit and inhibit, respectively, thalamic neurons via GABAergic cells in the SNr. Subsequent gating of afferent signal transduction through the thalamus could influence sensory responses of neocortical neurons.

Dopamine-dependent modulation of corticostriatal synaptic efficacy plays the essential role in selection of neocortical activity by the BG (Atallah et al., 2004, Gurney et al., 2001, Hikosaka et al., 2000, Silkis, 2001, Sil’kis, 2003, Sil’kis, 2006). Selection in these models is triggered by dopaminergic (DA) cell firing in response to conditioned stimulation. However, the dopamine, BG and particularly, the striatum participate in coding non-rewarding salient visual stimuli as well (Mele et al., 2004, Zink et al., 2003). The precise mechanism of the BG and dopamine involvement in visual processing was unknown. However, the understanding the function of the BG may help to explain the origin of some deficits in visual perception following a lesion or degeneration of the visual striatum (Jacobs et al., 1995). Therefore, the first goal of the present work was to define the mechanisms underlying the contribution of visual and limbic C-BG-Th-C loops and dopamine to visual processing.

The attentional selection of incoming information for further analysis plays a central role in processing, since it controls access to restricted capabilities of the sensory processing system. Visual attention can be captured by salient stimuli (bottom-up control), or it may be voluntarily directed to a particular stimulus location or feature (top-down control). Recent studies reveal some properties of visual attention that operates through facilitation of visual processing of the attended stimulus and inhibition of representations of unattended stimuli in primary V1 and higher visual cortical areas (Di Russo et al., 2003, Mehta et al., 2000, Treue, 2001). Dopamine plays a significant role in regulation of attention, since damage of dopaminergic input suppresses attentional effects, while dopamine receptor agonists reduce attentional deficit (Nieoullon, 2002). It is widely assumed that attentional modulation reflects the action of cortico-cortical feedback projections. However, it is unclear how the neocortical targets for amplification and suppression by attention could be found by these projections. Further, what mechanisms underlie this suppression and dopaminergic dependence of attention? The second goal of this work was to elucidate the mechanism underlying dopamine and C-BG-Th-C loop involvement in attentional effects.

Section snippets

Proposed mechanism of dopamine-dependent selection of neocortical activity by cortico-basal ganglia-thalamocortical loops

Recently we proposed a hypothetical mechanism underlying the participation of motor and limbic C-BG-Th-C loops, containing motor and prefrontal cortex (PFC), in dopamine-dependent conditioned selection of motor activity (Sil’kis, 2006). Taking into consideration the similarity of functional organization of the C-BG-Th-C loops involved in sensory and motor processing (Middleton and Strick, 1996), we assumed that mechanisms for selection of sensorimotor activity (Sil’kis, 2006) and visually

A hypothetical mechanism for involvement of cortico-basal ganglia-thalamocortical loops and dopamine in visual processing and its attentional modulation

A proposed mechanism for involvement of the BG and dopamine in visual processing and attention is based on the several principles.

Conclusions

Some principles of proposed mechanism of visual processing have been used in other models. However our current model has the following distinctions.

  • 1.

    Reentrant signaling in the cortex could be promoted by disinhibition through the C-BG-Th-C loop. In other models only reentrant signaling by the cortico-cortical and/or thalamocortical loops is considered.

  • 2.

    Selection of neuronal patterns representing visual stimuli in diverse neocortical areas is the result of dopamine-dependent modulation of

Acknowledgement

The author is very grateful to Dr. Gene Johnson, Charlottesville, Virginia, USA for his helpful comments, and for editing of this manuscript.

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