Responses of a looming-sensitive neuron to compound and paired object approaches

The lobula giant movement detector (LGMD) and its target neuron, the descending contralateral movement detector (DCMD), constitute a motion-sensitive pathway in the locust visual system that responds preferentially to objects approaching on a collision course. LGMD receptive field properties, anisotropic distribution of local retinotopic inputs across the visual field, and localized habituation to repeated stimuli suggest that this pathway should be sensitive to approaches of individual objects within a complex visual scene. We presented locusts with compound looming objects while recording from the DCMD to test the effects of nonuniform edge expansion on looming responses. We also presented paired objects approaching from different regions of the visual field at nonoverlapping, closely timed and simultaneous approach intervals to study DCMD responses to multiple looming stimuli. We found that looming compound objects evoked characteristic responses in the DCMD and that the time of peak firing was consistent with predicted values based on a weighted ratio of the half size of each distinct object edge and the absolute approach velocity. We also found that the azimuthal position and interval of paired approaches affected DCMD firing properties and that DCMDs responded to individual objects approaching within 106 ms of each other. Moreover, comparisons between individual and paired approaches revealed that overlapping approaches are processed in a strongly sublinear manner. These findings are consistent with biophysical mechanisms that produce nonlinear integration of excitatory and feed-forward inhibitory inputs onto the LGMD that have been shown to underlie responses to looming stimuli.     

Time-dependent activation of feed-forward inhibition in a looming-sensitive neuron

The lobula giant movement detector (LGMD) is an identified neuron in the locust visual system that responds preferentially to objects approaching on a collision course with the animal. For such looming stimuli, the LGMD firing rate gradually increases, peaks, and decays toward the end of approach. The LGMD receives both excitatory and feed-forward inhibitory inputs on distinct branches of its dendritic tree, but little is known about the contribution of feed-forward inhibition to its response properties. We used picrotoxin, a chloride channel blocker, to selectively block feed-forward inhibition to the LGMD. We then computed differences in firing rate and membrane potential between control and picrotoxin conditions to study the activation of feed-forward inhibition. For looming stimuli, a significant activation of inhibition was observed early, as objects exceeded on average approximately 23 degrees in angular extent at the retina. Inhibition then increased in parallel with excitation over the remainder of approach trials. Experiments in which the final angular size of the approaching objects was systematically varied revealed that the relative activation of excitation and inhibition remains well balanced over most of the course of looming trials. Feed-forward inhibition actively contributed to the termination of the response to approaching objects and was particularly effective for large or slowly moving objects. Suddenly appearing and receding objects activated excitation and feed-forward inhibition nearly simultaneously, in contrast to looming stimuli. Under these conditions, the activation of excitation and feed-forward inhibition was weaker than for approaching objects, suggesting that both are preferentially tuned to approaching objects. These results support a phenomenological model of multiplication within the LGMD and provide new constraints for biophysical models of its responses to looming and receding stimuli.     

Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. Selective responses to approaching objects.

1. The "descending contralateral movement detector" (DCMD) neuron in the locust has been challenged with a variety of moving stimuli, including scenes from a film (Star Wars), moving disks, and images generated by computer. The neuron responds well to any rapid movement. For a dark object moving along a straight path at a uniform velocity, the DCMD gives the strongest response when the object travels directly toward the eye, and the weakest when the object travels away from the eye. Instead of expressing selectivity for movements of small rather than large objects, the DCMD responds preferentially to approaching objects. 2. The neuron shows a clear selectivity for approach over recession for a variety of sizes and velocities of movement both of real objects and in simulated movements. When a disk that subtends > or = 5 degrees at the eye approaches the eye, there are two peaks in spike rate: one immediately after the start of movement; and a second that builds up during the approach. When a disk recedes from the eye, there is a single peak in response as the movement starts. There is a good correlation between spike rate and angular acceleration of the edges of the image over the eye. 3. When an object approaches from a distance sufficient for it to subtend less than one interommatidial angle at the start of its approach, there is a single peak in response. The DCMD tracks the approach, and, if the object moves at 1 m/s or faster, the spike rate increases throughout the duration of object movement. The size of the response depends on the speed of approach. 4. It is unlikely that the DCMD encodes the time to collision accurately, because the response depends on the size as well as the velocity of an approaching object. 5. Wide-field movements suppress the response to an approaching object. The suppression varies with the temporal frequency of the background pattern. 6. Over a wide range of contrasts of object against background, the DCMD gives a stronger response to approaching than to receding objects. For low contrasts, the selectivity is greater for objects that are darker than the background than for objects that are lighter.     

A looming-sensitive pathway responds to changes in the trajectory of object motion

Two identified locust neurons, the lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD), constitute one motion-sensitive pathway in the visual system that responds preferentially to objects that approach on a direct collision course and are implicated in collision-avoidance behavior. Previously described responses to the approach of paired objects and approaches at different time intervals (Guest BB, Gray JR. J Neurophysiol 95: 1428-1441, 2006) suggest that this pathway may also be affected by more complicated movements in the locust's visual environment. To test this possibility we presented stationary locusts with disks traveling along combinations of colliding (looming), noncolliding (translatory), and near-miss trajectories. Distinctly different responses to different trajectories and trajectory changes demonstrate that DCMD responds to complex aspects of local visual motion. DCMD peak firing rates associated with the time of collision remained relatively invariant after a trajectory change from translation to looming. Translatory motion initiated in the frontal visual field generated a larger peak firing rate relative to object motion initiated in the posterior visual field, and the peak varied with simulated distance from the eye. Transition from translation to looming produced a transient decrease in the firing rate, whereas transition away from looming produced a transient increase. The change in firing rate at the time of transition was strongly correlated with unique expansion parameters described by the instantaneous angular acceleration of the leading edge and subtense angle of the disk. However, response time remained invariant. While these results may reflect low spatial resolution of the compound eye, they also suggest that this motion-sensitive pathway may be capable of monitoring dynamic expansion properties of objects that change the trajectory of motion.     

Influence of electrotonic structure and synaptic mapping on the receptive field properties of a collision-detecting neuron

The lobula giant movement detector (LGMD) is a visual interneuron of Orthopteran insects involved in collision avoidance and escape behavior. The LGMD possesses a large dendritic field thought to receive excitatory, retinotopic projections from the entire compound eye. We investigated whether the LGMD's receptive field for local motion stimuli can be explained by its electrotonic structure and the eye's anisotropic sampling of visual space. Five locust (Schistocerca americana) LGMD neurons were stained and reconstructed. We show that the excitatory dendritic field and eye can be fitted by ellipsoids having similar geometries. A passive compartmental model fit to electrophysiological data was used to demonstrate that the LGMD is not electrotonically compact. We derived a spike rate to membrane potential transform using intracellular recordings under visual stimulation, allowing direct comparison between experimental and simulated receptive field properties. By assuming a retinotopic mapping giving equal weight to each ommatidium and equally spaced synapses, the model reproduced the experimental data along the eye equator, though it failed to reproduce the receptive field along the ventral-dorsal axis. Our results illustrate how interactions between the distribution of synaptic inputs and the electrotonic properties of neurons contribute to shaping their receptive fields.     

Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects.

1. We examine the critical image cues that are used by the locust visual system for the descending contralateral motion detector (DCMD) neuron to distinguish approaching from receding objects. Images were controlled by computer and presented on an electrostatic monitor. 2. Changes in overall luminance elicited much smaller and briefer responses from the DCMD than objects that appeared to approach the eye. Although a decrease in overall luminance might boost the response to an approaching dark object, movement of edges of the image is more important. 3. When two pairs of lines, in a cross-hairs configuration, were moved apart and then together again, the DCMD showed no preference for divergence compared with convergence of edges. A directional response was obtained by either making the lines increase in extent during divergence and decrease in extent during convergence; or by continually increasing the velocity of line movement during divergence and decreasing velocity during convergence. 4. The DCMD consistently gave a larger response to growing than to shrinking solid rectangular images. An increase compared with a decrease in the extent of edge in an image is, therefore, an important cue for the directionality of the response. For single moving edges of fixed extent, the neuron gave the largest response to edges that subtended 15 degrees at the eye. 5. The DCMD was very sensitive to the amount by which an edge traveled between frames on the display screen, with the largest responses generated by 2.5 degrees of travel. This implies that the neurons in the optic lobe that drive this movement-detecting system have receptive fields of about the same extent as a single ommatidium. 6. For edges moving up to 250 degree/s, the excitation of the DCMD increases with velocity. The response to an edge moving at a constant velocity adapts rapidly, in a manner that depends on velocity. Movement over one part of the retina can adapt the subsequent response to movement over another part of the retina. 7. For the DCMD to track and continue to respond to the image of an approaching object, the edges of the image must continually increase in velocity. This is the second important stimulus cue. 8. Edges of opposite contrasts (light-dark compared with dark-light) are processed in separate pathways that inhibit each other. This would contribute to the reduction of responses to wide-field movements.     

Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust

Locusts have two large collision-detecting neurons, the descending contralateral movement detectors (DCMDs) that signal object approach and trigger evasive glides during flight. We sought to investigate whether vision for action, when the locust is in an aroused state rather than a passive viewer, significantly alters visual processing in this collision-detecting pathway. To do this we used two different approaches to determine how the arousal state of a locust affects the prolonged periods of high-frequency spikes typical of the DCMD response to approaching objects that trigger evasive glides. First, we manipulated arousal state in the locust by applying a brief mechanical stimulation to the hind leg; this type of change of state occurs when gregarious locusts accumulate in high-density swarms. Second, we examined DCMD responses during flight because flight produces a heightened physiological state of arousal in locusts. When arousal was induced by either method we found that the DCMD response recovered from a previously habituated state; that it followed object motion throughout approach; and--most important--that it was significantly more likely to generate the maintained spike frequencies capable of evoking gliding dives even with extremely short intervals (1.8 s) between approaches. Overall, tethered flying locusts responded to 41% of simulated approaching objects (sets of 6 with 1.8 s ISI). When we injected epinastine, the neuronal octopamine receptor antagonist, into the hemolymph responsiveness declined to 12%, suggesting that octopamine plays a significant role in maintaining responsiveness of the DCMD and the locust to visual stimuli during flight.     

Impact of neural noise on a sensory-motor pathway signaling impending collision

Noise is a major concern in circuits processing electrical signals, including neural circuits. There are many factors that influence how noise propagates through neural circuits, and there are few systems in which noise levels have been studied throughout a processing pathway. We recorded intracellularly from multiple stages of a sensory-motor pathway in the locust that detects approaching objects. We found that responses are more variable and that signal-to-noise ratios (SNRs) are lower further from the sensory periphery. SNRs remain low even with the use of stimuli for which the pathway is most selective and for which the neuron representing its final sensory level must integrate many synaptic inputs. Modeling of this neuron shows that variability in the strength of individual synaptic inputs within a large population has little effect on the variability of the spiking output. In contrast, jitter in the timing of individual inputs and spontaneous variability is important for shaping the responses to preferred stimuli. These results suggest that neural noise is inherent to the processing of visual stimuli signaling impending collision and contributes to shaping neural responses along this sensory-motor pathway.     

Role of an identified looming-sensitive neuron in triggering a flying locust's escape

Flying locusts perform a characteristic gliding dive in response to predator-sized stimuli looming from one side. These visual looming stimuli trigger trains of spikes in the descending contralateral movement detector (DCMD) neuron that increase in frequency as the stimulus gets nearer. Here we provide evidence that high-frequency (>150 Hz) DCMD spikes are involved in triggering the glide: the DCMD is the only excitatory input to a key gliding motor neuron during a loom; DCMD-mediated EPSPs only summate significantly in this motor neuron when they occur at >150 Hz; when a looming stimulus ceases approach prematurely, high-frequency DCMD spikes are removed from its response and the occurrence of gliding is reduced; and an axon important for glide triggering descends in the nerve cord contralateral to the eye detecting a looming stimulus, as the DCMD does. DCMD recordings from tethered flying locusts showed that glides follow high-frequency spikes in a DCMD, but analyses could not identify a feature of the DCMD response alone that was reliably associated with glides in all trials. This was because, for a glide to be triggered, the high-frequency spikes must be timed appropriately within the wingbeat cycle to coincide with wing elevation. We interpret this as flight-gating of the DCMD response resulting from rhythmic modulation of the flight motor neuron's membrane potential during flight. This means that the locust's escape behavior can vary in response to the same looming stimulus, meaning that a predator cannot exploit predictability in the locust's collision avoidance behavior.     

Plasticity in the visual system is correlated with a change in lifestyle of solitarious and gregarious locusts

We demonstrate pronounced differences in the visual system of a polyphenic locust species that can change reversibly between two forms (phases), which vary in morphology and behavior. At low population densities, individuals of Schistocerca gregaria develop into the solitarious phase, are cryptic, and tend to avoid other locusts. At high densities, individuals develop instead into the swarm-forming gregarious phase. We analyzed in both phases the responses of an identified visual interneuron, the descending contralateral movement detector (DCMD), which responds to approaching objects. We demonstrate that habituation of DCMD is fivefold stronger in solitarious locusts. In both phases, the mean time of peak firing relative to the time to collision nevertheless occurs with a similar characteristic delay after an approaching object reaches a particular angular extent on the retina. Variation in the time of peak firing is greater in solitarious locusts, which have lower firing rates. Threshold angle and delay are therefore conserved despite changes in habituation or behavioral phase state. The different rates of habituation should contribute to different predator escape strategies or flight control for locusts living either in a swarm or as isolated individuals. For example, increased variability in the habituated responses of solitarious locusts should render their escape behaviors less predictable. Relative resistance to habituation in gregarious locusts should permit the continued responsiveness required to avoid colliding with other locusts in a swarm. These results will permit us to analyze neuronal plasticity in a model system with a well-defined and controllable behavioral context.     

The responsiveness of Clare-Bishop neurons to motion cues for motion stereopsis

Under paralysis of eye movement and optical adjustment of visual axes of the two eyes, neuronal responsiveness in cat Clare-Bishop (CB) cortex to the binocular presentation of visual stimuli was studied using two types of visual stimulator which presented: 3-dimensional motion of a visual stimulus; and the motion cues (movement of retinal images in the two eyes) contained in the 3-dimensional motion. On the basis of the responsiveness to 3-dimensional motion presented by the first type of stimulator, the CB cells were classified into approaching (AP) cells which were selectively responsive to the approaching motion of a visual stimulus, recessive (RC) cells responsive to the recessive motion, frontoparallel (FP) cells responsive to the frontoparallel motion and non-selective (NS) cells responsive to more than two types of motion. The investigation of the CB cells with 2-dimensional motion stimulus demonstrated 3 different types of binocular interaction: facilitatory (52/239); antagonistic (33/239) or linear summation (154/239). Cells exhibiting the facilitatory interaction (n = 52) were all FP cells, those exhibiting the antagonistic interaction were either AP (n = 25) or RC cells (n = 8), and those exhibiting the linear summation were comprised of all varieties of cells (49 AP, 17 RC, 31 FP and 57 NS cells). The cells responsive to the approaching (37 AP cells) or recessive motion between the center of the receptive area and the nose (10 RC cells), or frontoparallel motion (42 FP cells) in the horizontal direction exhibited the selective responsiveness to the motion disparity (a combination of horizontal movement of retinal images in the two eyes), and those responsive to the vertically or obliquely deviating approaching (20 AP cells) or recessive motion (14 RC cells), or frontoparallel motion in the vertical or oblique directions (13 FP cells) exhibited that for a combination of the motion disparity and the frontoparallel motion in the vertical or oblique direction. These findings indicate that the CB cell responsiveness to 3-dimensional motion of a visual stimulus is explained by the binocular integration of motion signal viewed by each eye.     

Spike-frequency adaptation and intrinsic properties of an identified, looming-sensitive neuron

We investigated in vivo the characteristics of spike-frequency adaptation and the intrinsic membrane properties of an identified, looming-sensitive interneuron of the locust optic lobe, the lobula giant movement detector (LGMD). The LGMD had an input resistance of 4-5 MOmega, a membrane time constant of about 8 ms, and exhibited inward rectification and rebound spiking after hyperpolarizing current pulses. Responses to depolarizing current pulses revealed the neuron's intrinsic bursting properties and pronounced spike-frequency adaptation. The characteristics of adaptation, including its time course, the attenuation of the firing rate, the mutual dependency of these two variables, and their dependency on injected current, closely followed the predictions of a model first proposed to describe the adaptation of cat visual cortex pyramidal neurons in vivo. Our results thus validate the model in an entirely different context and suggest that it might be applicable to a wide variety of neurons across species. Spike-frequency adaptation is likely to play an important role in tuning the LGMD and in shaping the variability of its responses to visual looming stimuli.     

Improved visual sensitivity during smooth pursuit eye movements

When we view the world around us, we constantly move our eyes. This brings objects of interest into the fovea and keeps them there, but visual sensitivity has been shown to deteriorate while the eyes are moving. Here we show that human sensitivity for some visual stimuli is improved during smooth pursuit eye movements. Detection thresholds for briefly flashed, colored stimuli were 16% lower during pursuit than during fixation. Similarly, detection thresholds for luminance-defined stimuli of high spatial frequency were lowered. These findings suggest that the pursuit-induced sensitivity increase may have its neuronal origin in the parvocellular retino-thalamic system. This implies that the visual system not only uses feedback connections to improve processing for locations and objects being attended to, but that a whole processing subsystem can be boosted. During pursuit, facilitation of the parvocellular system may reduce motion blur for stationary objects and increase sensitivity to speed changes of the tracked object.     

The temporal pattern of motion in depth perception derived from ERPs in humans

Former studies have demonstrated the cortical regions being involved in visual motion processing. The strength of neuronal activation was found to depend on the direction of motion. In particular the detection of optic flow towards the observer seems of particular importance due to its obvious biological relevance. We used event related potentials (ERPs) to add data of the temporal dynamics of this neuronal processing. Using current density reconstruction, source maxima of differential activation in motion in depth versus planar motion in the time range from 50 to 400 ms after stimulus onset were localized, and the time courses of activation were elaborated. Source reconstruction revealed six regions contributing significant source activity related to the perception of motion in depth: occipital pole, bilateral fusiform gyrus, right lateral superior occipital cortex and bilateral superior parietal cortex. Our data provide evidence for an early involvement of visual occipital cortex in the perception of motion in depth stimuli, followed by activation within parietal cortex, presumably associated with attention information processing. Sub-dividing the effects of the direction of the stimuli in motion in depth perception, optic flow directed towards the observer-induced stronger activation, but this differential activation excluded the parietal cortex. Thus the temporal deconvolution of the electrophysiological data suggests that the differential processing of approaching stimuli is initiated at an early stage of visual perception within the visual association area.     

Heat stress-mediated plasticity in a locust looming-sensitive visual interneuron

Neural circuits are strongly affected by temperature and failure ensues at extremes. However, detrimental effects of high temperature on neural pathways can be mitigated by prior exposure to high, but sublethal temperatures (heat shock). Using the migratory locust, Locusta migratoria, we investigated the effects of heat shock on the thermosensitivity of a visual interneuron [the descending contralateral movement detector (DCMD)]. Activity in the DCMD was elicited using a looming stimulus and the response was recorded from the axon using intracellular and extracellular methods. The thoracic region was perfused with temperature-controlled saline and measurements were taken at 5 degrees intervals starting at 25 degrees C. Activity in DCMD was decreased in control animals with increased temperature, whereas heat-shocked animals had a potentiated response such that the peak firing frequency was increased. Significant differences were also found in the thermosensitivity of the action potential properties between control and heat-shocked animals. Heat shock also had a potentiating effect on the amplitude of the afterdepolarization. The concurrent increase in peak firing frequency and maintenance of action potential properties after heat shock could enhance the reliability with which DCMD initiates visually guided behaviors at high temperature.     

Distribution of optokinetic sensitivity across the retina of mice in relation to eye orientation

We examined the effects of stimulus size and location on the mouse optokinetic response (OKR). To this end, we recorded initial OKRs elicited by a brief presentation of horizontally moving grating patterns of different vertical widths and locations in the visual field. Large-field stimuli generated large sustained OKRs, whereas visual stimuli of narrower vertical widths elicited weaker sustained responses at the later period (400–500 ms after the onset of stimulus motion). However, even stimuli of only 5° vertical width elicited detectable transient responses at the initial open-loop period (100–200 ms after the onset of stimulus motion). Presenting 5°-width stimuli at different vertical locations (−10° to +35° relative to the horizon) revealed the spatial distribution of optokinetic sensitivity across the retina. The most sensitive part of the visual field was located at +25°. In addition, we examined the vertical orientation of the eye under our stereotaxic set-up. We observed the optic disc using a hand-held fundus camera and determined the ocular orientation. All eye orientations were distributed in the range of +20–30° relative to the horizon (25.2±2.5°). Thus, the direction of the most sensitive visual field matched the angle of eye orientation. These findings indicate that the spatial distribution of visual field sensitivity to optokinetic stimuli coincides with the distribution of retinal ganglion cell density.     

Recruitment of local inhibitory networks by horizontal connections in layer 2/3 of ferret visual cortex

To investigate how neurons in cortical layer 2/3 integrate horizontal inputs arising from widely distributed sites, we combined intracellular recording and voltage-sensitive dye imaging to visualize the spatiotemporal dynamics of neuronal activity evoked by electrical stimulation of multiple sites in visual cortex. Individual stimuli evoked characteristic patterns of optical activity, while delivering stimuli at multiple sites generated interacting patterns in the regions of overlap. We observed that neurons in overlapping regions received convergent horizontal activation that generated nonlinear responses due to the emergence of large inhibitory potentials. The results indicate that co-activation of multiple sets of horizontal connections recruit strong inhibition from local inhibitory networks, causing marked deviations from simple linear integration.     

Smooth-pursuit eye movements elicited by first-order and second-order motion

 The perception of the displacement of luminance-defined contours (i.e., first-order motion) is an important and well-examined function of the visual system. It can be explained, for example, by the operation of elementary motion detectors (EMDs), which cross-correlate the spatiotemporal luminance distribution. More recent studies using second-order motion stimuli, i.e., shifts of the distribution of features such as contrast, texture, flicker, or motion, extended classic concepts of motion perception by including nonlinear or hierarchical processing in the EMD. Smooth-pursuit eye movements can be used as a direct behavioral probe for motion processing. The ability of the visual system to extract motion signals from the spatiotemporal changes of the retinal image can be addressed by analyzing the elicited eye movements. We measured the eye movement response to moving objects defined by two different types of first-order motion and two different types of second-order motion. Our results clearly showed that the direction of smooth-pursuit eye movements was always determined by the direction of object motion. In particular, in the case of second-order motion stimuli, smooth-pursuit did not follow the retinal image motion. The latency of the initial saccades during pursuit of second-order stimuli was slightly but significantly increased, compared with the latency of saccades elicited by first-order motion. The processing of second-order motion in the peripheral visual field was less exact than the processing of first-order motion in the peripheral field. Steady state smooth-pursuit eye speed did not reflect the velocity of second-order motion as precisely as that of first-order motion, and the resulting retinal error was compensated by saccades. Interestingly, for slow second-order stimuli we observed that the eye could move faster than the target, leading to small, corrective saccades in the opposite direction to the ongoing smooth-pursuit eye movement. We conclude from our results that both visual perception and the control of smooth-pursuit eye movements have access to processing mechanisms extracting first- and second-order motion. Received: 26 August 1996 / Accepted: 8 November 1996     

Sensory versus motor loci for integration of multiple motion signals in smooth pursuit eye movements and human motion perception

We have investigated how visual motion signals are integrated for smooth pursuit eye movements by measuring the initiation of pursuit in monkeys for pairs of moving stimuli of the same or differing luminance. The initiation of pursuit for pairs of stimuli of the same luminance could be accounted for as a vector average of the responses to the two stimuli singly. When stimuli comprised two superimposed patches of moving dot textures, the brighter stimulus suppressed the inputs from the dimmer stimulus, so that the initiation of pursuit became winner-take-all when the luminance ratio of the two stimuli was 8 or greater. The dominance of the brighter stimulus could be not attributed to either the latency difference or the ratio of the eye accelerations for the bright and dim stimuli presented singly. When stimuli comprised either spot targets or two patches of dots moving across separate locations in the visual field, the brighter stimulus had a much weaker suppressive influence; the initiation of pursuit could be accounted for by nearly equal vector averaging of the responses to the two stimuli singly. The suppressive effects of the brighter stimulus also appeared in human perceptual judgments, but again only for superimposed stimuli. We conclude that one locus of the interaction of two moving visual stimuli is shared by perception and action and resides in local inhibitory connections in the visual cortex. A second locus resides deeper in sensory-motor processing and may be more closely related to action selection than to stimulus selection.