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Figure 10 Retinal image stabilization during head rotation. As the head rotates about its vertical axis, the eyes reflexively rotate in the opposite direction to stabilize gaze, the direction of the eye in space. The two sinusoidal plots show the angular direction of the head in space (top) and the eye in its orbit (middle). The flat summation of these changes (bottom) signifies a steady gaze despite movements of the head.

cerebral activation revealed by functional magnetic resources imaging during simple and complex visuo-motor tasks.

A few behavioral facts about saccades must be presented before considering their neural circuitry. First, saccades are open loop (i.e., ballistic and preprogrammed). As Gerald Westheimer stated, ''once initiated, saccadic movements complete their predetermined course and cannot be modified or countermanded.'' In fact, 50-100 msec prior to its start, the saccade generally cannot be canceled or redirected on the basis of new sensory information. Second, saccades have long reaction times. Saccadic latency, the time from the appearance of an unpredictable visual target to the start of the movement, is 100-400 msec (200 msec being typical). Third, saccades have a long refractory period. It is usually difficult to initiate a second saccade for 100-200 ms after the previous saccadic movement ends. Fourth, saccades are highly stereotyped movements. Thus, the saccadic waveform and its parameters (duration, velocity, etc.) are almost completely determined by the dimensions of the movement vector being programmed. Finally, although saccades to foveate a stimulus can seem reflexive, and have been termed the visual grasp reflex, one can make accurate and advantageous predictive saccades that anticipate where a stimulus will appear. Thus, saccades can be guided by our experience, memories, guesses, purposes, and strategies as well as by overt visual stimulation.

1. The Saccade Generator

The first four properties mentioned previously reflect the fact that all saccades are ultimately ''generated'' or programmed in a very rigid, mechanistic fashion by a specialized circuit in the brain stem. This final common pathway for all rapid eye movements, called the saccade generator, is a network of several distinctive types of neurons embedded within the reticular formation near the oculomotor nuclei. This network originally evolved to generate the quick-phase movements of vestibulooptokinetic nystagmus. Thus, voluntary saccades of primates are accomplished by the relatively new FS triggering this ISS circuitry. If the saccade generator is damaged, then all rapid eye movements, both reflexive and voluntary, are disabled.

To accomplish a saccadic eye movement, the OMNs of the agonist muscle(s) need a special waveform of innervation: a pulse followed by a step. The pulse is a brief period of spiking at a very high rate, which is used to move the eye very quickly to its new location. The step is the new level of tonic discharge needed to hold the eye at its new location in the orbit. This pulse-step innervation is inherent in the OMN equation given earlier, and is illustrated in Fig. 11. Not shown is the fact that the pulse briefly but completely silences most OMNs of the antagonist muscles via inhibitory interneurons termed inhibitory burst neurons. This brief silence is also inherent in the basic OMN equation reviewed previously.

The pulse is provided by the principal output neuron of the saccade generator—the excitatory burst neuron (EBN). EBNs discharge with a high-frequency burst of spikes in conjunction with all saccadic eye movements and are silent between saccades. Their bursts begin b 12 msec before the eye starts to move (they have also been called short-lead bursters) and end just before the eye completes the saccade. Horizontal EBNs are located in the caudal portion of the paramedian pontine reticular formation, conveniently near the abducens nucleus. Their spike counts during each burst determine the horizontal displacement of the saccade (in the ipsilateral direction). Vertical EBNs are located in the rostral interstitial nucleus of the medial longitudinal fasciculus, with separate sets of neurons for the upward and downward components. Other EBNs here also represent torsional saccadic eye movements.

The tonic ''step'' change in the OMN innervation is provided by the neural integrator that adds the pulse (EBN spikes) to its current value and then maintains that new value. Thus, when each saccade is made, the

Figure 11 Pulse-step innervation of oculomotor neurons. A schematic showing eye position (top) and spike rates of burst and tonic neurons (middle) for real and hypothetical conditions producing abnormal and normal saccades. (Left) Given pulse activity but no tonic activity (step) to defend the new eye position, the eye slides back to its starting position (e.g., gaze-evoked nystagmus). (Middle) In the hypothetical case of a damaged pulse generator, the tonic/step activity alone causes very slow eye movements that ''glide'' exponentially to a target. (Bottom) Circuit diagram for pulse-step innervation of oculomotor neurons and the generation of saccades. The excitatory burst neurons are activated by signals from higher levels (e.g., the superior colliculus and frontal eye field). The activity of tonic neurons reflects ongoing integration of all eye velocity commands by neural integrator circuits in the pons and midbrain. Oculomotor neurons sum these phasic and tonic inputs to produce a highvelocity saccade and then to hold this new eye position.

Figure 11 Pulse-step innervation of oculomotor neurons. A schematic showing eye position (top) and spike rates of burst and tonic neurons (middle) for real and hypothetical conditions producing abnormal and normal saccades. (Left) Given pulse activity but no tonic activity (step) to defend the new eye position, the eye slides back to its starting position (e.g., gaze-evoked nystagmus). (Middle) In the hypothetical case of a damaged pulse generator, the tonic/step activity alone causes very slow eye movements that ''glide'' exponentially to a target. (Bottom) Circuit diagram for pulse-step innervation of oculomotor neurons and the generation of saccades. The excitatory burst neurons are activated by signals from higher levels (e.g., the superior colliculus and frontal eye field). The activity of tonic neurons reflects ongoing integration of all eye velocity commands by neural integrator circuits in the pons and midbrain. Oculomotor neurons sum these phasic and tonic inputs to produce a highvelocity saccade and then to hold this new eye position.

neural integrator quickly ''steps'' from its old pre-saccadic level of activity to a new postsaccadic level. In contrast, the response of the neural integrator to a low-velocity long-duration signal from the VOR command is a ''ramp'' change in output rate. This short-term memory mechanism has been successfully modeled with recurrent neural networks and thus is schematized as a single recurrent feedback connection (Fig. 8C).

Several cell types antecedent to the EBNs have been identified. One of the most remarkable types is the omnipause neuron (OPN). The tonic activity of these inhibitory (glycine) neurons has the critical job of keeping all EBNs totally silent during the intervals between saccades. If EBNs had even a low spontaneous rate when not bursting, then the neural integrator would generate random ''walks'' between saccades instead of providing steady fixations. Only when OPNs temporarily stop spiking (which they briefly do in conjunction with all saccades, regardless of saccade size or direction) are EBNs given an opportunity to discharge. In fact, electrical stimulation at the OPN locus (nucleus raphe interpositus along the midline of the pons) during a saccadic eye movement will immediately brake the eye and (prematurely) end the saccade, and continuous stimulation there prevents all rapid eye movements, but not slow eye movements, such as the VOR or smooth pursuit. Detailed consideration of OPNs and the other cell types that complete the saccade generator circuit are beyond the scope of this article.

2. Visually Guided Saccades and the Superior Colliculus

How can the brain stem's saccade generator be activated to produce useful saccades in the absence of head movements and VO/OK stimulation? The exemplar structure for this function is the superior colliculus (SC), which forms the roof of the midbrain. The SC is the mammalian version of the optic tectum, which is the vertebrate brain's prototype sensorimotor structure. The SC receives a strong projection directly from the retina as well as afferents from most other senses (auditory, somatosensory, etc.), and its efferents to the brain stem and spinal cord serve to orient the head and body toward localized sensory inputs. In the primate, and other mammals with a foveation system, a major role of the SC is to move visual stimuli appearing in the visual periphery into the foveal region of the retina by triggering a saccadic eye movement of the appropriate size and direction. This automatic, visually guided foveating saccade has been called the visual grasp reflex.

The functional anatomy of the primate SC that affords such visually guided foveation is forthright (Fig. 12): Neurons in the superficial layer of the primate SC constitute a topographic map of the contralateral visual hemifield (Fig. 12B; interestingly, this is only true of primates—for all other vertebrates each SC represents the entire contralateral eye). Neurons in the deeper, intermediate layer of the primate SC provide a topographic map of all contralateral^ directed saccade vectors. These sensory and

Figure 12 Spatial-to-temporal transformation of saccade vectors. Depiction of the necessity of a spatial-to-temporal transformation as saccade commands are relayed from the superior colliculus (SC) to the saccade generator, but the figure does not show how it is accomplished. (A) Spatial representation of four hypothetical visual stimuli. The stimuli are within the central-most 10° of the diagram and the dashed lines lead to enlargement of this region. (B) A visuotopic map of the SCshowing the idealized representations of the visual stimuli depicted in A on the surface of the SC. Note that more than half the SCis used to map the central 10° (adapted with permission from M. CynaderandN. Berman, J. Neurophysiol. 35,187,1972). (C) Saccade-related burst cells in the deeper SC layers code saccadic eye movements via their location in its spatial map of the contralateral visual hemifield. The top two traces are horizontal and vertical eye coordinates, and the bottom traces are spikes. These cells burst most robustly prior to a saccade matching their preferred vector (reprinted from D. L. Sparks, Brain Res. 156,1, copyright 1978, with permission from Elsevier Science). (D) Hypothetical response of the excitatory burst neurons (EBNs), the output stage of the saccade generator, to the visual stimuli shown in A and B. Top traces are eye position, and lower traces are the bursts of horizontal (Hor) EBNs [in the caudal paramedian pontine reticular formation (PPRF)] and vertical (Ver) EBNs [in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF)]. Saccade dimensions are a quasilinear function of the number of spikes in the bursts. Since EBNs usually burst at near-maximal rates, their spike count is largely a function of burst duration, just as saccade size is largely a function of saccade duration. In contrast, the burst duration of the saccade-related bursters in the SC is independent of saccade size or duration.

Figure 12 Spatial-to-temporal transformation of saccade vectors. Depiction of the necessity of a spatial-to-temporal transformation as saccade commands are relayed from the superior colliculus (SC) to the saccade generator, but the figure does not show how it is accomplished. (A) Spatial representation of four hypothetical visual stimuli. The stimuli are within the central-most 10° of the diagram and the dashed lines lead to enlargement of this region. (B) A visuotopic map of the SCshowing the idealized representations of the visual stimuli depicted in A on the surface of the SC. Note that more than half the SCis used to map the central 10° (adapted with permission from M. CynaderandN. Berman, J. Neurophysiol. 35,187,1972). (C) Saccade-related burst cells in the deeper SC layers code saccadic eye movements via their location in its spatial map of the contralateral visual hemifield. The top two traces are horizontal and vertical eye coordinates, and the bottom traces are spikes. These cells burst most robustly prior to a saccade matching their preferred vector (reprinted from D. L. Sparks, Brain Res. 156,1, copyright 1978, with permission from Elsevier Science). (D) Hypothetical response of the excitatory burst neurons (EBNs), the output stage of the saccade generator, to the visual stimuli shown in A and B. Top traces are eye position, and lower traces are the bursts of horizontal (Hor) EBNs [in the caudal paramedian pontine reticular formation (PPRF)] and vertical (Ver) EBNs [in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF)]. Saccade dimensions are a quasilinear function of the number of spikes in the bursts. Since EBNs usually burst at near-maximal rates, their spike count is largely a function of burst duration, just as saccade size is largely a function of saccade duration. In contrast, the burst duration of the saccade-related bursters in the SC is independent of saccade size or duration.

motor maps are in perfect register for making foveat-ing saccades. For example, if recording from a superficial layer neuron located near the center of the left SC, the visual response field center would be 10° right of the fixation point (cross in Fig. 12B). If the microelectrode were then advanced into the underlying intermediate layer, it would record a ''saccade-related burst neuron'' that responds optimally (i.e., has the most spikes in its burst) immediately prior to 10° rightward saccades (Fig. 12C), exactly the saccade needed to foveate visual stimuli appearing in the superficial (layer) neuron's visual response field (RF). Moreover, electrical stimulation there would yield a 10° rightward saccade as well.

3. Transformation from Spatial Code to Temporal Code

Saccades are clearly ''spatially'' coded in the SC in that the saccade vector is determined by which part of collicular ''space'' has active saccade-related bursters. In contrast, the output cells of the saccade generator, the EBNs, use a ''temporal'' code for saccade metrics: Saccade size is coded by the spike counts in their bursts (Fig. 12D) and not by which (or where) EBNs are spiking most. Exactly how this spatial-to-temporal transformation is carried out is unclear. Moreover, the cortical eye field signals need the same spatial-to-temporal transformation, and neither the cortex nor the colliculus projects directly to the EBNs. Another class of saccade generator neurons, the long-lead burst neurons (LLBNs), seem to be an intermediate stage in this transformation. LLBNs do receive direct projections from the SC and FEF. Moreover, individual LLBNs often prefer saccades with specific oblique directions and amplitudes, like SC and FEF neurons but unlike EBNs.

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