Changes in sensory responsivity in deep layer neurons of the superior colliculus of behaving rats

Beha vioural Brain Research, 47 (1992) 97-10 I 9 1992 Elsevier Science Publishers B.V. All rights reserved. 0166-4328/92/S05.00

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Changes in sensory responsivity in deep layer neurons of the superior colliculus of behaving rats Douglas A. Weldon ~ and Phillip J. Best 2 IDepartment of Psycholog~v, Hamilton College, Clinton. NY 13323 (U.S.A.) and 2Department of Psychology, University of New Orleans, New Orleans. LA 70148 (U.S.A.) (Received 26 August 1991) (Revised version received 10 November 1991) (Accepted 27 November 1991)

Key words: Superior colliculus; Single-unit activity; Sensory receptive field

Neurons in the deep layers of the superior colliculus in behaving hooded rats were tested for responsivity to visual, auditory, or somesthetic stimuli. Some sensory cells, particularly those responsive to tactile stimuli, showed a change in responsivity (and sometimes an abolishment in firing rate or a change in receptive field size) when the animal was gently restrained or placed onto an elevated platform. Thus, sensory qeurons in the superior colliculus of the behaving rat have response properties that vary according tp.._the conditions of testing.

As a recipient of sensory information of several modalities and the source of efferents that connect with brainstem areas involved in eye, head, and neck movemerits, the mammalian superior colliculus (SC) holds promise as one of the brain locations where the process of sensorimotor integration will be understood. The deep layers ofthis area contain neurons that are responsive to auditory, visual, and tactile stimuli, and some that are multimodal t2. The receptivity of these cells, however, is not static but is dynamic. In behaving cats and monkeys the sensoritopic map varies according to the motor actions that are being executed 6"8. In monkeys, visually responsive neurons located in the superficial layers of the SC show enhanced responsiveness when the stimulus is a target for an eye movemerit ~5. The present research examined the characteristics of single neurons in the SC in behaving rats. In this species, a role for the SC in attentional and visuomotor processing has been inferred from lesion and stimulation studies, but there is remarkably little evidence from Correspondence: D.A. Weldon, Department of Psychology, I lamilton College, Clinton, NY 13323, USA.

neurophysiological studies in behaving animals. One notable exception is the documentation of rat SC cells firing in relation to sensory and motor events in a study of neural correlates of fighting behavior 9. Our findings indicate that the responsivities in sensory neurons of the SC of behaving rats are not fixed, and that they change when the animals are moving or are gently restrained. The experimental animals used in this study were 16 male Long-Evans hooded rats of body weights ranging between 300 and 450 g at the time of surgery. Animals were tested in a wooden box 40 cm high with an open top 59 • 35 cm and the floor 30 • 35 cm. The two side walls were placed at a 60 ~ angle (sloping outwards from the bottom of the box to the top) to prevent the animal from contacting its electrode connector against them while moving. A video camera photographed the animal's behavior head-on through the clear front panel made of 23 mm clear acrylic. Each animal received, while under pentobarbital anesthesia, an intracranial implant of a moveable microelectrode consisting of 10 nichrome mierowires 25 Imi in diameter 3-7. The microelectrode assemblies, constructed with 1-72 screws, allowed total excursions of 2 mm in increments of approxitnately 20 itm. Elec-

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Fig. !. A: photomicrograph of a coronal section through the SC in one of the animais'ifi the present study showifig'an electrode track from one of the microelectrode bundles. B: superimposed action potentials measured from a single unit in the behaving rat.

99 trophysiological signals were amplified at the head via source follower transistors, passed to Grass P 15 microelectrode preamplifiers and then to Bak differential amplifiers. Amplification levels were 10,000 gain with half-amplitude low frequency cutoffs at 300 Hz and high frequency cutoffs at 3 kHz for single unit signals. Data were then stored on videocassette (Vetter Model 420) for later analysis. Three days following electrode placement, animals were tested while connected to the source-follower and commutator system. Electrophysiological and behavioral data were recorded on videocassette for later analysis off-line. In searching for single units, electrode bundles were lowered in depths of 30 lira and the animals were observed while engaging in spontaneous activity in the testing apparatus and while visual, auditory, and tactile stimuli were presented. Each cell was isolated with action potentials that met the criterion of 3 : 1 signal/noise ratio. For sensory responsiveness testing, stimuli of several modalities were presented to the animal as it explored the testing apparatus with room lights on. Visual responsiveness was tested by presenting a 3 cm white circular disk to the visual fields while the room lights were on or by flashing a penlight to the visual fields while the animal was in the dark. Auditory sensitivity was evaluated by jingling keys, snapping fingers, and brushing a card against the wooden box. Somatosensory responsiveness was tested by touching the animal with a camel hair brush or gently tapping the skin with the eraser end of a pencil. Sections of video tape were played and signals were passed into a Bak window discriminator and time delay circuit to ensure that action potentials analyzed were from a single unit (as defined by identical amplitude and time course characteristics). Signals were sent from the Bak window discriminator output to an Apple IIe

TABLE I

Summary of characteristics of single neurons recorded in the present

Slltdy Total (distinct units) Neurons with sensory rcsponsivity Unimodal Visual responsivity Auditory responsivity Tactile responsivity Bimodal VA VT AT Trimodal

56 27 3 1 12 3 5 1 2

microcomputer which stored the data on disks for subsequent analysis. Histological verification of cannula and electrode positions indicated that the electrodes through which the 56 units were recorded were in the intermediate and deep layers of the SC (see Fig. 1A for an example). An example of a recording from a single unit in the SC of the unrestrained rat is presented in Fig. lB. A total of 27 cells (48~o) showed clear evidence of sensory responsiveness. Ofthese cells, 13 showed visual responsivity, 7 showed auditory responsivity, and 20 showed tactile responsivity. The unimodal and multimodal characteristics are indicated in Table I. Most neurons recorded were silent until an effective stimulus was presented. In 9 of the 20 cells with tactile receptivity, the response changed with the behavioral testing situation. In these neurons, the responsivity when the animal was moving freely in the cage was reduced when the rat was gently restrained in the experimenter's hand; some of the neurons lost all responsivity. The effects in each of the two testing conditions were immediate (see Fig. 2). Responsivity was also fo~fad t6 be reduced in one of the visual cells tested (see Fig. 3). The fact that this reduction in activity was not related to a simple loss of the cell by injury or electrode movement was indicated by the fact that the activity returned when the animal was allowed to run freely (see Figs. 2 and 3). The immediate reduction in responsivity by the restraint and the immediate recovery upon release indicates that the effects were not simply attributable to habituation. To determine whether manual restraint was a necessary feature of the condition causing responsivity to change, one of the tactile cells was tested when the animal was placed on a platform suspended from the ceiling of the testing chamber. In this cell there was again a clear reduction in responsivity in the platform condition in comparison with the situation where the animal was freely moving in the box. The receptive field size became reduced (see Fig. 4) such that the oro-facial and vibrissae responsiveness in the free exploration condition became reduced to oral responsivity when the animal was on the platform. The present results demonstrate that the deep layers of the SC in behaving rats have neurons that respond to visual, auditory, and tactile stimuli, as has been demonstrated for anesthetized rodents (rats ~~ mice 2, and hamsters 1'4'13'14) and other mammalian species (for review see ref. 12). The sensory receptivity of those neurons, however, can change as a function of the behavioral parameters of the testing situation. Of the neurons that showed sensory recel6tivity to tactile information, 45 %,, showed clear evidence of such a change

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Fig. 2. A 3 - m i n u t e record of r e s p o n s e s o f a d e e p layer S C cell to a tactile s t i m u l u s p r e s e n t e d to the vibrissae w h e n t h e animal was m o v i n g in the testing box (dark arrows) or held in the e x p e r i m e n t e r ' s h a n d (light arrows). Stimulation reliably p r o d u c e d a cellular r e s p o n s e w h e n the a n i m a l w a s freely m o v i n g , but a r e s p o n s e was elicited only 5 0 ~ o f the time w h e n t h e animal was held in t h e hand. T h e return o f reliable r e s p o n s e s to tactile s t i m u l a t i o n following r e p l a c e m e n t in the t e s t i n g box indicates that the reduction o f responsivity w a s not d u e to electrode m o v e m e n t o r n e u r o n a l habituation.

a receptive field when another stimtdus is prcseulcd outside the rcccptive field at the same time II. There are ttndottbtedly--many determinants of changes in receptivity characteristics of collicular neurons. In behaving monkeys, sensory stimuli elicit stronger responses from collicular neurons when they are the targets for subsequent saccades than when they are not ~s. Some monkey SC neurons fire in response to a localized auditory stimulus only when the monkey's eyes are in a particular orbital position; movement of the eyes to a different position produces an apparent shift in the attditory receptive field ~'. Similar alterations of SC neuron rcccptivity to visual stimuli with direction of gaze occur in cat SC cells ~. Additional research is required to t, nderstand the particular features of the present testing situation that were rcsponsible for the

with the simple manipulation of holding the animal in the hand. In every case in which we observed that modnlation, the SC ccll activity was reduced when the animal was gently restrained in the hand in comparison with the freely moving state. This cffcct can also be generalized to other brain systems, since a similar reduction in hippocampal place cell activity occurs during physical restraint in rats 5. In SC cells, other conditions lead to this modulation besides manual restraint; cell activity can be reduced when the activity of the animal is restricted by the stnall size of the platform that it is bahmcing upon. This result indicates that, at least for some neurons, the change in sensitivity is probably not related to the stimulation by the hand of areas outside the receptive field. Thus, the effect is not an example of the change in response to a stimtdtts inside

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T i m e (1 s e c p e r division) Fig. 3. Rate of firingofa dccp la3er SC neuron to a stilnulus card repeatedly presented t o tile visual receptive field xvhilctile animal was freely moving (sections under tile black rectangles) or gently restrained in the experimenter's hand (sections under the cross-hatchcd rectangle). Rcsponsivity to the visual stimulus was essentially abolished in the manual restraint condition.

I01 tion o f s o m e o f the electrodes for the r e c o r d i n g s m a d e in this study.

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REFERENCES

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Fig. 4. Reduction of the size of a receptive fieldas a function of the

conditions of testing. In the top picture, the animal was tested in a freely behaving situation without restraint. Action potentials were obtained by stimulating the skin around the mouth with a camel hair brush. In the bottom illustration, the responsivity of the cell was eliminated when the animal was held in the experimenter's hand. In the middle, the animal was placed on an elevated platform, thereby providing the same height and limited movement as in the lower figure, except without the grasp of the experimenter. In this case the receptive field was reduced in size, but the cell still fired in response to the stimulation.

c h a n g e s in responsivity and receptive fields a n d to d o c u m e n t the specific affercnts 1o the S C that are involved in this m o d u l a t i o n o f collicuhtr activity. This r e s e a r c h was s u p p o r t e d by N I M H 1-F32M H 0 9 5 1 3 - 0 1 a n d a faculty fellowship f r o m H a m i l t o n College. P a r t o f the r e s e a r c h w a s c o n d u c t e d while D . A . W . w a s a visiting s c h o l a r a n d P.J.B. w a s P r o f e s s o r oi" P s y c h o l o g y at the University o f Virginia. T h e a u t h o r s w o u l d like to express their t h a n k s to S t e p h e n l ' u l l m a n for his technical assistance in building the l a b o r a t o r y at H a m i l t o n College and to K i m b e r l y Preucil for c o n s t r u e -

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