Response Normalization in the Superficial Layers of the Superior Colliculus as a Possible Mechanism for Saccadic Averaging

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 06/2014; 34(23):7976-7987. DOI: 10.1523/JNEUROSCI.3022-13.2014
Source: PubMed


How does the brain decide where to look? Neuronal networks within the superior colliculus (SC) encode locations of intended eye movements. When faced with multiple targets, the relative activities of neuronal populations compete for the selection of a saccade. However, the computational principles underlying saccadic choices remain poorly understood. We used voltage imaging of slices of rat SC to record circuit dynamics of population responses to single- and dual-site electrical stimulation to begin to reveal some of the principles of how populations of neurons interact. Stimulation of two distant sites simultaneously within the SC produced two distinct peaks of activity, whereas stimulation of two nearby sites simultaneously exhibited a single, merged peak centered between the two sites. The distances required to produce merged peaks of activity corresponded to target separations that evoked averaging saccades in humans performing a corresponding dual target task. The merged activity was well accounted for by a linear weighed summation and a divisive normalization of the responses evoked by the single-site stimulations. Interestingly, the merging of activity occurred within the superficial SC, suggesting a novel pathway for saccadic eye movement choice.

Download full-text


Available from: Corinne R. Esquibel, Nov 06, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Multiple visual stimuli are common in natural scenes, yet it remains unclear how multiple stimuli interact to influence neuronal responses. We investigated this question by manipulating relative signal strengths of two stimuli moving simultaneously within the receptive fields (RFs) of neurons in the extrastriate middle temporal (MT) cortex. Visual stimuli were overlapping random-dot patterns moving in two directions separated by 90°. We first varied the motion coherence of each random-dot pattern and characterized, across the direction tuning curve, the relationship between neuronal responses elicited by bi-directional stimuli and by the constituent motion components. The tuning curve for bi-directional stimuli showed response normalization and can be accounted for by a weighted sum of the responses to the motion components. Allowing nonlinear, multiplicative interaction between the two component responses significantly improved the data fit for some neurons and the interaction mainly had a suppressive effect on the neuronal response. The weighting of the component responses was not fixed, but dependent on relative signal strengths. When two stimulus components moved at different coherence levels, the response weight for the higher-coherence component was significantly greater than that for the lower-coherence component. We also varied relative luminance levels of two coherently moving stimuli and found that MT response weight for the higher-luminance component was also greater. These results suggest that competition between multiple stimuli within a neuron's RF depends on relative signal strengths of the stimuli, and that multiplicative nonlinearity may play an important role in shaping the response tuning for multiple stimuli.
    Preview · Article · Jun 2014 · Journal of Neurophysiology
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The superior colliculus, or tectum, is a key sensorimotor structure that long predates the cortex. In this issue of Neuron, Zhao et al. (2014) show that the visual cortex controls the tectum’s gain precisely and retinotopically, without otherwise altering its operations.
    Full-text · Article · Oct 2014 · Neuron
  • [Show abstract] [Hide abstract]
    ABSTRACT: Abstract Purpose: Glaucoma is a group of optic neuropathies characterized by the loss of retinal ganglion cells (RGCs). Since ocular hypertension (OHT) is a main risk factor, current therapies are predominantly based on lowering eye pressure. However, a subset of treated patients continues to lose vision. More research into pathological mechanisms underlying glaucoma is therefore warranted in order to develop novel therapeutic strategies. In this study we investigated the impact of OHT from eye to brain in mice. Methods: Monocular hypertension (mOHT) was induced in CD-1 mice by laser photocoagulation (LP) of the perilimbal and episcleral veins. The impact on the retina and its main direct target area, the superficial superior colliculus (sSC), was examined via immunostainings for Brn3a, VGluT2 and GFAP. Alterations in neuronal activity in V1 and extrastriate areas V2L and V2M were assessed using in situ hybridization for the activity reporter gene zif268. Results: Transient mOHT resulted in diffuse and sectorial RGC degeneration. In the sSC contralateral to the OHT eye, a decrease in VGluT2 immunopositive synaptic connections was detected one week post LP, which appeared to be retinotopically linked to the sectorial RGC degeneration patterns. In parallel, hypoactivity was discerned in contralateral retinotopic projection zones in V1 and V2. Despite complete cortical reactivation 4 weeks post LP, in the sSC no evidence for recovery of RGC synapse density was found and also the concomitant inflammation was not completely resolved. Nevertheless, sSC neurons appeared healthy upon histological inspection and subsequent analysis of cell density revealed no differences between the ipsi- and contralateral sSC. Conclusion: In addition to RGC death, OHT induces loss of synaptic connections and neuronal activity in the visual pathway and is accompanied by an extensive immune response. Our findings stress the importance of looking beyond the eye and including the whole visual system in glaucoma research.
    No preview · Article · Jan 2015 · Current Eye Research
Show more