A multimodal pathway including the basal ganglia in the feline brain

The purpose of this paper is to give an overview of our present knowledge about the feline tecto-thalamo-basal ganglia cortical sensory pathway. We reviewed morphological and electrophysiological studies of the cortical areas, located in ventral bank of the anterior ectosylvian sulcus as well as the region of the insular cortex, the suprageniculate nucleus of the thalamus, caudate nucleus, and the substantia nigra. Microelectrode studies revealed common receptive field properties in all these structures. The receptive fields were extremely large and multisensory, with pronounced sensitivity to motion of visual stimuli. They often demonstrated directional and velocity selectivity. Preference for small visual stimuli was also a frequent finding. However, orientation sensitivity was absent. It became obvious that the structures of the investigated sensory loop exhibit a unique kind of information processing, not found anywhere else in the feline visual system.

Joint representation of translational and rotational components of optic flow in parietal cortex

Terrestrial navigation naturally involves translations within the horizontal plane and eye rotations about a vertical (yaw) axis to track and fixate targets of interest. Neurons in the macaque ventral intraparietal (VIP) area are known to represent heading (the direction of self-translation) from optic flow in a manner that is tolerant to rotational visual cues generated during pursuit eye movements. Previous studies have also reported that eye rotations modulate the response gain of heading tuning curves in VIP neurons. We tested the hypothesis that VIP neurons simultaneously represent both heading and horizontal (yaw) eye rotation velocity by measuring heading tuning curves for a range of rotational velocities of either real or simulated eye movements. Three findings support the hypothesis of a joint representation. First, we show that rotation velocity selectivity based on gain modulations of visual heading tuning is similar to that measured during pure rotations. Second, gain modulations of heading tuning are similar for self-generated eye rotations and visually simulated rotations, indicating that the representation of rotation velocity in VIP is multimodal, driven by both visual and extraretinal signals. Third, we show that roughly one-half of VIP neurons jointly represent heading and rotation velocity in a multiplicatively separable manner. These results provide the first evidence, to our knowledge, for a joint representation of translation direction and rotation velocity in parietal cortex and show that rotation velocity can be represented based on visual cues, even in the absence of efference copy signals.

Responses of MST neurons to plaid stimuli

The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway.

FM velocity selectivity in the inferior colliculus is inherited from velocity-selective inputs and enhanced by spike threshold

Frequency modulation (FM) is computed from the temporal sequence of activated auditory nerve fibers representing different frequencies. Most studies in the inferior colliculus (IC) have inferred from extracellular recordings that the precise timing of nonselective inputs creates selectivity for FM direction and velocity (Andoni S, Li N, Pollak GD. J Neurosci 27: 4882–4893, 2007; Fuzessery ZM, Richardson MD, Coburn MS. J Neurophysiol 96: 1320–1336, 2006; Gordon M, O'Neill WE. Hear Res 122: 97–108, 1998). We recently reported that two additional mechanisms were more important than input timing for directional selectivity in some IC cells: spike threshold and inputs that were already selective (Gittelman JX, Li N, Pollak GD. J Neurosci 29: 13030–13041, 2009). Here, we show that these same mechanisms, selective inputs and spike threshold, underlie selectivity for FM velocity and intensity. From whole cell recordings in awake bats, we recorded spikes and postsynaptic potentials (PSPs) evoked by downward and upward FMs that swept identical frequencies at different velocities and intensities. To determine the synaptic mechanisms underlying PSP selectivity (relative PSP height), we derived sweep-evoked synaptic conductances. Changing FM velocity or intensity changed conductance timing and size. Modeling indicated that excitatory conductance size contributed more to PSP selectivity than conductance timing, indicating that the number of afferent spikes carried more FM information to the IC than precise spike timing. However, excitation alone produced mostly suprathreshold PSPs. Inhibition reduced absolute PSP heights, without necessarily altering PSP selectivity, thereby rendering some PSPs subthreshold. Spike threshold then sharpened selectivity in the spikes by rectifying the smaller PSPs. This indicates the importance of spike threshold, and that inhibition enhances selectivity via a different mechanism than previously proposed.

Neural Mechanisms of Stimulus Velocity Tuning in the Superior Colliculus

Superior colliculus (SC)–mediated control of visuomotor behavior depends on neuronal selectivity for stimulus velocity. However, the mechanism responsible for velocity tuning in SC neurons is unclear. It was shown in a previous study of anesthetized, decorticate hamsters that the number and distribution of feed-forward retinal inputs are not critical for velocity tuning. Here the alternate hypothesis that inhibition from the surround determines velocity tuning of SC neurons was tested. Surround inhibition was present in 65% (43/66) of SC neurons recorded in the superficial gray layer. Neurons within this group that were selective for slowly moving stimuli exhibited spatially asymmetric surround inhibition, and their velocity tuning arose by preferential suppression of responses to rapidly moving stimuli. In the other 35% (23/66) of SC neurons recorded, surround inhibition was weak or absent and did not play a role in velocity tuning. Most neurons with surround inhibition were nonselective for the duration of stationary flashed stimuli, whereas neurons without surround inhibition were selective for stimulus duration. The majority of neurons that preferred intermediate or rapidly moving stimuli exhibited spatially symmetric surround inhibition. In these neurons, occluding the surround reduced velocity selectivity by enhancing responses to slowly moving stimuli. Based on these data, a model is proposed suggesting spatiotemporal interactions between inhibition and excitation that could underlie velocity tuning.