Effects of Focal Inactivation of Dorsal or Ventral Layers of the Lateral Geniculate Nucleus on Cats' Ability to See and Fixate Small Targets
Andrew K. Tate1, 2 and
Joseph G. Malpeli2
1 Neuroscience Program and 2 Department of Psychology, University of Illinois, Champaign, Illinois 61820
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ABSTRACT |
Tate, Andrew K. and Joseph G. Malpeli. Effects of focal inactivation of dorsal or ventral layers of the lateral geniculate nucleus on cats' ability to see and fixate small targets. J. Neurophysiol. 80: 2206-2209, 1998. To reveal contributions of different subdivisions of the lateral geniculate nucleus (LGN) to visuomotor behavior, segments of either layer A or the C layers were inactivated with microinjections of
-aminobutyric acid while cats made saccades to retinally stabilized spots of light placed either in affected regions of visual space or mirror-symmetric locations in the opposite hemifield. Inactivating layer A reduced the success rate for saccades to targets presented in affected locations from 82.4 to 26.8% while having no effect on saccades to the control hemifield. Saccades to affected sites had reduced accuracy and longer initiation latency and tended to be hypometric. In contrast, inactivating C layers did not affect performance. Data from all conditions fell along the same saccade velocity/amplitude function ("main sequence"), suggesting that LGN inactivations cause localization deficits, but do not interfere with saccade dynamics. Cerebral cortex is the only target of the A layers, so behavioral decrements caused by inactivating layer A must be related to changes in cortical activity. Inactivating layer A substantially reduces the activity of large subsets of corticotectal cells in areas 17 and 18, whereas few corticotectal cells depend on C layers for visually driven activity. The parallels between these behavioral and electrophysiological data along with the central role of the superior colliculus in saccadic eye movements suggests that the corticotectal pathway is involved in both deficits and remaining capacities resulting from blockade of layer A.
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INTRODUCTION |
The cat lateral geniculate nucleus (LGN) is comprised of a dorsal pair of layers (A and A1 for contralateral and ipsilateral eyes, respectively), a ventral complex of four strata (C, C1, C2, and C3), and the medial interlaminar nucleus. The A layers are the largest subdivision, and their inactivation causes the most dramatic reductions of cortical activity (e.g., Malpeli et al. 1986
). Nevertheless, considerable activity survives layer-A inactivation in area 17 (Malpeli 1983
, 1986; Weyand et al. 1986
), area 18 (Lee et al. 1998b
; Weyand et al. 1991
), and the lateral suprasylvian visual area (Lee et al. 1998a
). Until now, no information was available on perceptual consequences of these interventions. Here we take the first steps linking LGN layers to behavior in cats by examining the effects of inactivating segments of layer A or the C layers as a group on saccades to visual targets.
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METHODS |
Data were obtained from two cats whose eye positions were monitored with the double magnetic induction method (Bour et al. 1984
). Fixation targets (laser spots) were positioned on a rear-projection screen by computer-steered mirror galvanometers. At trial start, a central target appeared, and if it was fixated within 4 s (±1.5-2.0° tolerance) a peripheral target appeared after a variable delay (300-1,000 ms). Saccades had to be launched within 1,500 ms of target onset, and targets acquired within 200 ms of saccade start (trials with double saccade were discarded); a generous tolerance window (±2.0-3.5°) was allowed to avoid discouraging the animal should inactivations degrade accuracy. Central fixation spots stayed on until a saccade was launched from the central tolerance window so the animal could not know when a peripheral target appeared without seeing it. To accustom the animal to the absence of a peripheral target (should inactivations make them invisible), in 20% of training and practice trials, no target appeared, and a reward was given for maintaining central fixation for a variable period after target acquisition (1,800-2,500 ms).
While the eye wandered about the central fixation point, peripheral targets were kept centered on the affected region of visual space by dynamic stabilization. For 4° shifts in eye position (the largest allowed by the tolerance window), stabilization was within 0.25° (0.03° position resolution plus 0.22° because of time lags). Stabilization was turned off when a saccade took the eye out of the central tolerance window, but by this time stabilization had already displaced the target from where it was when the saccade was launched. Therefore, to avoid inducing hypermetric saccades, while the eye was in flight targets were returned to the location they occupied at saccade start.
During training and practice sessions, targets were drawn pseudorandomly from a continually changing set whose eccentricities covered the range employed in injection sessions and whose inclinations spanned a wider range, including the vertical meridian. During inactivation sessions, two targets were presented in pseudorandom order, one centered on the receptive-field location of activity recorded at the injection site and one in the mirror-symmetric location in the other hemifield. Receptive-field locations were determined by computer-automated mapping with narrow, retinally stabilized vertical and horizontal bars rapidly flashed on and off in a rectilinear grid. Their eccentricity ranged from 4.4 to 13.2°; all were within 4° of the horizontal meridian; none were closer than 4.4° from the vertical meridian. Any errors in calibrating the eye-position recording system were inconsequential because they were identical (and thus offsetting) for localizing receptive fields and peripheral targets.
Usually, several practice sessions were interspersed between injection sessions. The locations of targets in practice and injection sessions were unrelated, so the former gave the animal no information about the latter. Inactivation periods were brief and constituted <0.1% of the time devoted to training and practice, so they were unlikely to have impacted learned behavior.
Synaptic transmission was reversibly blocked by injecting 120 nl of
-amino-n-butyric acid (25 mM in saline) (Merigan et al. 1991b
) into sites located by recording LGN activity. Injections were made remotely, without suspending the task, interrupting data collection, or disturbing the animal (Fig. 1).

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| FIG. 1.
System for recording and injecting through micropipettes, adapted from one designed for microelectrodes (Malpeli et al. 1992 ). Miniature microdrive (Deadwyler et al. 1979 ) screws onto an adapter (a) rigidly connected to a guide tube (b) passing through a cylindrical base (c) cemented to the skull. The guide tube is trapped by a low-melting point alloy filling the base (not shown); it can be redirected when the alloy is melted. A stepping motor (not shown) is connected by a telescoping shaft and universal joints (d) to an eccentric cylinder (e). This cylinder rotates on an axle rigidly attached to the microdrive by a locking nut (not shown) on the threaded barrel, driving the microdrive thimble via an O-ring belt (f) to advance the micropipette. Belt slippage is inconsequential because micropipette depth is monitored with a charge-coupled device camera. A sleeve made from hypodermic tubing (g) protects the micropipette and holds a scale for tracking movement of fluid via the camera. Short lengths of hypodermic tubing (h) cemented to the micropipette reinforce critical points. An adapter fitted to the micropipette (not shown) provides electrical contact for recording and an air-tight seal to polyethylene tubing for pressure-injecting drugs. Components sterilized by heat or (for drugs) microfiltration. Drawing not to scale; diameter of implanted cylinder is ~5 mm.
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Surgeries were performed aseptically under barbiturate anesthesia (thiopental sodium) supplemented by buprenorphine (0.0075 mg/kg). Treatment of animals was in accordance with guidelines of the American Physiological Society (for more detail see Lee and Malpeli 1998
). Statistical significance was determined by permutation tests; all comparisons are between the 120 s preceding and the 110 s after injection.
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RESULTS |
Inactivating either layer A or the C layers did not interfere with acquiring central fixation points and holding them while awaiting the appearance of peripheral targets (Fig. 2, top left). When layer A was inactivated and targets in affected locations were viewed through the contralateral eye, the reward rate dropped substantially for about 110 s (82.4% normal; 26.8% blocked; P < 0.000001) and then rapidly recovered (Fig. 2, top right). No saccades were made to affected targets in 54.1% of trials; saccades were made toward or away from targets for 40.9 and 5.0% of trials, respectively (Fig. 3, left). During layer-A inactivation, saccades had lower amplitude (7.95° normal; 6.60° blocked; P < 0.0001), correspondingly lower peak velocity (218.4°/s normal; 183.9°/s blocked; P < 0.0001), and much longer latency (317.5 ms normal; 513.6 ms blocked; P < 0.0001); they were also less tightly grouped than saccades before inactivation (Fig. 3, left). For viewing through the ipsilateral eye, there was no deficiency after layer-A inactivation, indicating that the drug did not penetrate adjacent layer A1 (Fig. 2, bottom left; P = 0.20). Inactivating the C layers had little effect on reward rate (Fig. 2, bottom right), saccade amplitude (6.42° normal; 6.94° blocked; P = 0.23), saccade peak velocity (156.2°/s normal; 155.0°/s blocked; P = 0.43), or saccade latency (314.7 ms normal; 324.8 ms blocked; P = 0.05). Across conditions, performance early in the session was somewhat better for the control hemifield than the affected hemifield (Fig. 2). This might reflect idiosyncratic asymmetries in the behavior of these cats, but it could also be due to accumulated damage to the experimental hemisphere. The peak-velocity/amplitude data fell along a single "main sequence" (Bahill et al. 1975
) for all conditions (Fig. 3, right).

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| FIG. 2.
Effects of lateral geniculate nucleus inactivations (all began at 0 s) on performance in saccade task. Data are binned into 10-s intervals and boxcar-averaged over 3 intervals. Number of trials in parentheses. Top left: success rate for acquiring and holding the central fixation point until peripheral target onset for targets viewed through the contralateral eye. Only trials that progressed to this stage were further analyzed. Top right: rate at which rewarded saccades were made during 25 layer-A inactivations for targets presented to the contralateral eye in the affected region of space or in the mirror-symmetric region. Bottom left: reward rate during 14 layer-A inactivations for targets presented to the ipsilateral eye. Bottom right: reward rate during 8 C-layer inactivations for targets presented to the contralateral eye.
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| FIG. 3.
Left: end points of saccades before (Layer A Normal) and during (Layer A Blocked) layer-A inactivation for trials in which targets were presented in the experimental hemifield; an equal number of targets to the other hemifield (saccades not shown) was pseudorandomly interwoven with these. Target position varied considerably across sessions, but to enable the global pattern to be easily grasped the data are presented as if targets were at a single location to the right at the mean azimuth (7.89°) and elevation ( 1.03° down) of all targets used; end points of individual saccades are rescaled accordingly. Saccade end point was taken as the location where eye velocity dropped below 10°/s. Crosses indicate size and location of tolerance windows around the central fixation point and peripheral target. Right: peak-velocity/amplitude function for saccades before and during inactivation (slope = 19.9 s 1, intercept = 52.3°/s; r = 0.894).
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DISCUSSION |
These data demonstrate that cortical activity surviving layer-A inactivation is insufficient for normal saccade performance, whereas activity dependent on the C layers is not critical for saccades to small targets. Although layer-A inactivation caused a substantial deficit, saccades were still made toward affected target locations~40% of the time (Fig. 3, left). The remaining performance could not have been achieved by guessing: with the target in an affected region of space, guessing could result in saccades to the correct hemifield only 50% of the time, whereas in fact 89.1% were directed toward the target. Furthermore, with guessing, saccade latency must increase linearly with target onset delay, yet the trend was opposite to this; mean latencies were 450.9, 492.3, 490.4, and 523.6 ms for delays of 300, 500, 700, and 1,000 ms, respectively.
Because the data for all conditions fall along the same "main sequence," it is unlikely that LGN inactivations interfered with motor circuits controlling saccade dynamics. More likely, layer-A inactivation degraded the ability to see and/or localize targets, accounting for the reduced frequency and accuracy of saccades. Why these saccades were on average hypometric is not clear. Cats tend to make hypometric saccades unless pushed for accuracy, and the reduced saccade amplitude may have been secondary to reduced target visibility, combined with the large tolerance window.
The LGN projects only to cortex, so the behavioral deficits must have been mediated by changes in cortical activity. Given the importance of the superior colliculus in saccade generation, these changes likely involved the corticotectal pathway, and previous investigations of corticotectal cells (Weyand et al. 1986
, 1991
) support this premise. Inactivating the C layers has relatively little effect on corticotectal cells, mirroring the lack of behavioral effects. In contrast, many corticotectal cells in areas 17 and 18 depend on layer A for visually driven activity, and these could account for the behavioral deficits during layer-A inactivation. Many others respond vigorously without layer-A input, and these might support the remaining saccades. Nothing is known of the dependence of corticotectal cells on individual LGN layers beyond areas 17 and 18, but these probably play a critical role in directing saccades. Indeed, the lateral suprasylvian visual area appears more important than areas 17 and 18 for visual orientation (Hardy and Stein 1988
; Payne et al. 1996
).
This is the first use of reversible inactivation techniques for revealing contributions of LGN layers to behavior. Permanent, fiber-sparing lesions (e.g., Merigan et al. 1991a
,b
; Schiller et al. 1990
) provide more time to evaluate resulting deficits. On the other hand, with reversible inactivations, the nature of the deficit is unlikely to be obscured by the plastic reorganization of associated neural circuits that sometimes follows permanent lesions.
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ACKNOWLEDGEMENTS |
We thank D. Lee, J. Park, and T. Weyand whose efforts in preliminary experiments allowed critical technical problems to be identified and overcome, and W. Busen for programming support and advice on the manuscript.
This work was supported by National Eye Institute Grant EY-02695.
Address for reprint requets: J. G. Malpeli, Dept. of Psychology, University of Illinois, 603 East Daniel St., Champaign, IL 61820.
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FOOTNOTES |
Received 3 April 1998; accepted in final form 17 June 1998.
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