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The Journal of Neuroscience, May 13, 2009, 29(19):6336-6347; doi:10.1523/JNEUROSCI.4815-08.2009

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Behavioral/Systems/Cognitive
Short-Latency Activation of Striatal Spiny Neurons via Subcortical Visual Pathways

Jan M. Schulz,¹ Peter Redgrave,² Carsten Mehring,³ Ad Aertsen,³ Koreen M. Clements,¹ Jeff R. Wickens,^1,4 and John N. J. Reynolds¹

¹Department of Anatomy and Structural Biology, School of Medical Sciences, University of Otago, Dunedin 9016, New Zealand, ²Department of Psychology, University of Sheffield, Western Bank, Sheffield S10 2TP, United Kingdom, ³Fakultät für Biologie and Bernstein Center for Computational Neuroscience, Albert-Ludwigs-Universität, 79104 Freiburg, Germany, and ⁴Okinawa Institute of Science and Technology, Uruma, Okinawa 904-2234, Japan

Correspondence should be addressed to Dr. John N. J. Reynolds, Department of Anatomy and Structural Biology, School of Medical Sciences, University of Otago, P.O. Box 913, Dunedin 9016, New Zealand. Email: john.reynolds@stonebow.otago.ac.nz

The striatum is a site of integration of neural pathways involved in reinforcement learning. Traditionally, inputs from cerebral cortex are thought to be reinforced by dopaminergic afferents signaling the occurrence of biologically salient sensory events. Here, we detail an alternative route for short-latency sensory-evoked input to the striatum requiring neither dopamine nor the cortex. Using intracellular recording techniques, we measured subthreshold inputs to spiny projection neurons (SPNs) in urethane-anesthetized rats. Contralateral whole-field light flashes evoked weak membrane potential responses in approximately two-thirds of neurons. However, after local disinhibitory injections of the GABA_A antagonist bicuculline into the deep layers of the superior colliculus (SC), but not the overlying visual cortex, strong, light-evoked, depolarizations to the up state emerged at short latency (115 ± 14 ms) in all neurons tested. Dopamine depletion using -methyl-para-tyrosine had no detectable effect on striatal visual responses during SC disinhibition. In contrast, local inhibitory injections of GABA agonists, muscimol and baclofen, into the parafascicular nucleus of the thalamus blocked the early, visual-evoked up-state transitions in SPNs. Comparable muscimol-induced inhibition of the visual cortex failed to suppress the visual responsiveness of SPNs induced by SC disinhibition. Together, these results suggest that short-latency, preattentive visual input can reach the striatum not only via the tecto-nigro-striatal route but also through tecto-thalamo-striatal projections. Thus, after the onset of a biologically significant visual event, closely timed short-latency thalamostriatal (glutamate) and nigrostriatal (dopamine) inputs are likely to converge on striatal SPNs, providing depolarizing and neuromodulator signals necessary for synaptic plasticity mechanisms.

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Received Oct. 6, 2008; revised March 19, 2009; accepted April 9, 2009.

Correspondence should be addressed to Dr. John N. J. Reynolds, Department of Anatomy and Structural Biology, School of Medical Sciences, University of Otago, P.O. Box 913, Dunedin 9016, New Zealand. Email: john.reynolds@stonebow.otago.ac.nz

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