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.     

Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron

The lobula giant movement detector (LGMD) in the locust visual system and its target neuron, the descending contralateral movement detector (DCMD), respond to approaching objects looming on a collision course with the animal. They thus provide a good model to study the cellular and network mechanisms underlying the sensitivity to this specific class of behaviorally relevant stimuli. We determined over an entire locust eye the density distribution of optical axes describing the spatial organization of local inputs to the visual system and compared it with the sensitivity distribution of the LGMD/DCMD to local motion stimuli. The density of optical axes peaks in the equatorial region of the frontal eye. Local motion sensitivity, however, peaks in the equatorial region of the caudolateral visual field and only correlates positively with the dorso-ventral density of optical axes. On local stimulation, both the velocity tuning and the response latency of the LGMD/DCMD depend on stimulus position within the visual field. Spatial and temporal integration experiments in which several local motion stimuli were activated either simultaneously or at fixed delays reveal that the LGMD processes local motion in a strongly sublinear way. Thus the neuron's integration properties seem to depend on several factors including its dendritic morphology, the local characteristics of afferent fiber inputs, and inhibition mediated by different pathways or by voltage-gated conductances. Our study shows that the selectivity of this looming sensitive neuron to approaching objects relies on more complex biophysical mechanisms than previously thought.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

20 Hz membrane potential oscillations are driven by synaptic inputs in collision-detecting neurons in the frog optic tectum

Although the firing patterns of collision-detecting neurons have been described in detail in several species, the mechanisms generating responses in these neurons to visual objects on a collision course remain largely unknown. This is partly due to the limited number of intracellular recordings from such neurons, particularly in vertebrate species. By employing patch recordings in a novel integrated frog eye-tectum preparation we tested the hypothesis that OFF retinal ganglion cells were driving the responses to visual objects on a collision course in the frog optic tectum neurons. We found that the majority (22/26) of neurons in layer 6 responding to visual stimuli fitted the definition of η class collision-detectors: they readily responded to a looming stimulus imitating collision but not a receding stimulus (spike count difference ∼10 times) and the spike firing rate peaked after the stimulus visual angle reached a threshold value of ∼20–45°. In the majority of these neurons (15/22) a slow frequency oscillation (f = ∼20 Hz) of the neuronal membrane potential could be detected in the responses to a simulated collision stimulus, as well as to turning off the lights. Since OFF retinal ganglion cells could produce such oscillations, our observations are in agreement with the hypothesis that ‘collision’ responses in the frog optic tectum neurons are driven by synaptic inputs from OFF retinal ganglion cells.     

Responses of primate visual cortical V4 neurons to simultaneously presented stimuli

We report here results from 45 primate V4 visual cortical neurons to the preattentive presentations of seven different patterns located in two separate areas of the same receptive field and to combinations of the patterns in the two locations. For many neurons, we could not determine any clear relationship for the responses to two simultaneous stimuli. However, for a substantial fraction of the neurons we found that the firing rate was well modeled as the maximum firing rate of each stimulus presented separately. It has previously been proposed that taking the maximum of the inputs ("MAX" operator) could be a useful operation for neurons in visual cortex, although there has until now been little direct physiological evidence for this hypothesis. Our results here provide direct support for the hypothesis that the MAX operator plays a significant (although certainly not exclusive) role in generating the receptive field properties of visual cortical neurons.     

Activity of eye movement-related neurons in and near the interstitial nucleus of Cajal during sinusoidal vertical linear acceleration and optokinetic stimuli

Summary 1. A total of 43 neurons that showed a close correlation with vertical eye movement with a burst-tonic or tonic type response during spontaneous saccades, were recorded within, and in the close vicinity of, the interstitial nucleus of Cajal (INC) in alert cats. Neuronal responses to sinusoidal vertical linear acceleration (0.2–0.85 Hz, amplitude 10.5 cm) and optokinetic stimuli (0.1–1.0 Hz, amplitude 10.5 cm), were examined. 2. All 43 eye movement-related neurons responded to sinusoidal vertical linear acceleration in the presence of a stationary visual pattern in correlation to robust eye movement responses with compensatory phase. Phase and gain values (re stimulus position) of response of individual cells were independent of the stimulus frequencies tested. Of these, 33 cells were examined during linear acceleration without visual input. Most cells (27/33) did not respond even when a weak linear vestibulo-ocular reflex was present (6/27). The remaining 6 cells (6/33) responded to linear acceleration. Their mean phase values advanced by 80 ° and gain dropped by 55% compared to the responses with visual inputs. 3. Twenty eight of the 43 cells were examined during vertical optokinetic stimuli. The activity of all 28 cells was modulated in correlation to eye movement responses. Response phase showed more lag, and gain decreased as stimulus frequencies increased, similar to optokinetic eye movement responses. 4. The close correlation between the activity of eye movement-related neurons in the INC region and robust eye movements during linear acceleration with visual inputs and optokinetic stimuli suggest that these neurons are involved in some aspect of vertical eye position generation during such stimuli.     

Human eye movement response to z-axis linear acceleration: the effect of varying the phase relationships between visual and vestibular inputs

We investigated the effect of systematically varying the phase relationship between 0.5-Hz sinusoidal z-axis optokinetic (OKN) and linear acceleration stimuli upon the resulting vertical eye movement responses of five humans. Subjects lay supine on a linear sled which accelerated them sinusoidally along their z-axis at 0.4 g peak acceleration (peak velocity 1.25 m/s). A high-contrast, striped z-axis OKN stimulus moving sinusoidally at 0.5 Hz, 70°/s peak velocity was presented either concurrently or with the acceleration stimulus or alone. Subjects' vertical eye movements were recorded using scleral search coils. When stimuli were paired in the naturally occurring relationship (e.g., visual stripes moving upward paired with downward physical acceleration), the response was enhanced over the response to the visual stimulus presented alone. When the stimuli were opposed (e.g., visual stripes moving upward during upward physical acceleration, a combination that does not occur naturally), the response was not significantly different from the response to the visual stimulus presented alone. Enhancement was maximized when the velocities of the visual and motion stimuli were in their normal phase relationship, while the response took intermediate values for other phase relationships. The phase of the response depended upon the phase difference between the two inputs. We suggest that linear self-motion processing looks at agreement between the two stimuli — a sensory conflict model.     

Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate

1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Constraints on the source of short-term motion adaptation in macaque area MT. I. the role of input and intrinsic mechanisms

Neurons in area MT, a motion-sensitive area of extrastriate cortex, respond to a step of target velocity with a transient-sustained firing pattern. The transition from a high initial firing rate to a lower sustained rate occurs over a time course of 20-80 ms and is considered a form of short-term adaptation. The present paper asks whether adaptation is due to input-specific mechanisms such as short-term synaptic depression or if it results from intrinsic cellular mechanisms such as spike-rate adaptation. We assessed the contribution of input-specific mechanisms by using a condition/test paradigm to measure the spatial scale of adaptation. Conditioning and test stimuli were placed within MT receptive fields but were spatially segregated so that the two stimuli would activate different populations of inputs from the primary visual cortex (V1). Conditioning motion at one visual location caused a reduction of the transient firing to subsequent test motion at a second location. The adaptation field, estimated as the region of visual space where conditioning motion caused adaptation, was always larger than the MT receptive field. Use of the same stimulus configuration while recording from direction-selective neurons in V1 failed to demonstrate either adaptation or the transient-sustained response pattern that is the signature of short-term adaptation in MT. We conclude that the shift from transient to sustained firing in MT cells does not result from an input-specific mechanism applied to inputs from V1 because it operates over a wider range of the visual field than is covered by receptive fields of V1 neurons. We used a direct analysis of MT neuron spike trains for many repetitions of the same motion stimulus to assess the contribution to adaptation of intrinsic cellular mechanisms related to spiking. On a trial-by-trial basis, there was no correlation between number of spikes in the transient interval and the interval immediately after the transient period. This is opposite the prediction that there should be a correlation if spikes cause adaptation directly. Further, the transient was suppressed or extinguished, not delayed, in trials in which the neuron emitted zero spikes during the interval that showed a transient in average firing rate. We conclude that the transition from transient to sustained firing in neurons in area MT is caused by mechanisms that are neither input-specific nor controlled by the spiking of the adapting neuron. We propose that the short-term adaptation observed in area MT emerges from the intracortical circuit within MT.     

The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

 We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information. Received: 17 June 1996 / Accepted: 29 April 1997     

Role of sustained excitability of the leg motor cortex after transcranial magnetic stimulation in associative plasticity

Changes in the strength of corticospinal projections to muscles in the upper and lower limbs are induced in conscious humans after paired associative stimulation (PAS) to the motor cortex. We tested whether an intervention of PAS consisting of 90 low-frequency (0.1-Hz) stimuli to the common peroneal nerve combined with suprathreshold transcranial magnetic stimulation (TMS) produces specific changes to the motor-evoked potentials (MEPs) in lower leg muscles if the afferent volley from peripheral stimulation is timed to arrive at the motor cortex after TMS-induced firing of corticospinal neurons. Unlike PAS in the hand, MEP facilitation in the leg was produced when sensory inputs were estimated to arrive at the motor cortex over a range of 15 to 90 ms after cortical stimulation. We examined whether this broad range of facilitation occurred as a result of prolonged subthreshold excitability of the motor cortex after a single pulse of suprathreshold TMS so that coincident excitation from sensory inputs arriving many milliseconds after TMS can occur. We found that significant facilitation of MEP responses (>200%) occurred when the motor cortex was conditioned with suprathreshold TMS tens of milliseconds earlier. Likewise, it was possible to induce strong MEP facilitation (85% at 60 min) when afferent inputs were directly paired with subthreshold TMS. We argue that in the leg motor cortex, facilitation of MEP responses from PAS occurred over a large range of interstimulus intervals as a result of the paired activation of sensory inputs with sustained, subthreshold activity of cortical neurons that follow a pulse of suprathreshold TMS.