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Intracranial Potentials Correlated with an Event-Related Potential, P300, in the Cat

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Intracranial Potentials Correlated with an Event-Related Potential, P300, in the Cat Brain Research, 339 (1985) 27-38 27 Elsevier BRE 10855 Intracranial Potentials Correlated With an Event-Related Potential, P300, in the Cat THOMAS A. O'CONNOR and ARNOLD STARR Department of Neurology, University of California, Irvine, CA 92717 (U.S.A.) (Accepted October 9th, 1984) Key words: event related potential -- P300 -- cat -- cortex -- hippocampus Intracranial recordings of long-latency, event-related potentials were obtained from paralyzed, artificially respirated cats. A mod- ified oddball paradigm was employed in which cats were presented with a randomized series of two tones, a 'frequent' 4 kHz stimulus and a 'rare' 1 kHz stimulus. A tail shock was administered 700 ms after onset of the rare tone. Under these circumstances the stimulus elicited a positive component at the vertex similar to the human P300. Intracranial potentials associated with the rare tone usually manifested components of greater amplitude than did potentials associated with the frequent tone. A positive component occurring in latency between 200 and 350 ms only accompanied the presentation of the rare stimulus. The P300 component, which was positive at the dura, appeared as a negative component within a few millimeters of the surface over a wide area of the marginal and suprasylvian gyri. Changing the probability of the rare stimulus resulted in a reduction in the amplitudes of both the intracranial negative compo- nent and the P300 recorded at the skull. Components of large amplitude associated with the rare stimulus were obtained from the re- gion of the hippocampus. These components reversed polarity, sometimes more than once, as the electrode was advanced. Substantial latency differences were often observed between the P300 recorded at the skull and P300-1ike intracranial components associated with the rare stimulus. These results suggest that the cortices of the marginal and suprasylvian gyri and the hippocampal region contribute to the generation of the cat P300. INTRODUCTION recording sites have only infrequently been em- ployed in humans 13,15,27.32,34. The P300 is a late positive component of the aver- Models of the P300 with animals conditoned to re- aged event-related potential recorded from the scalp spond to the rare stimulus have been devel- of humans that reflects the expectancies of the sub- oped 2,3,7A°,16AS,21` but there are few reports of P300- ject rather than the physical parameters of the stimu- like potentials recorded from within the brain 10A~. In lus 6,28. These contingencies have led to the desig- this study a cat model, developed earlier in our labo- nation of the P300 as an 'endogenous component' of ratory 7`s, was employed. Cats exposed to a classical event-related potentials29. The amplitude of the P300 adversive conditioning paradigm showed a late posi- is inversely proportional to the global probability of tive component which had an average latency at the the stimulus 5.14.22 24,26 whereas its latency is related, midline of the skull of 260 ms. This component's am- in part, to task difficulty 9AI,25,26 and subject age 12. plitude was large when the signal was task relevant, Typically, subjects are asked to count rare stimuli, its amplitude varied inversely with stimulus probabil- which are randomly intermixed with a series of fre- ity, and it could be evoked by stimuli of different mo- quent stinmli. The rare stimulus evokes the P30(I. dalities 30, characteristics similar to the P300 in hu- Since this component is best elicited when the subject mans. The present study in the cat measures the po- is engaged in the task, the P300 is believed to reflect tentials at several intracranial locations at the time of cognitive events of information processing. Very the skull P300 event to help locate and characterize little, however, is known of the neural structures in- neural generators of this animal analogue of the hu- volved in generating the P300 since intracranial re- man P300. cordings and neuroanatomical identification of the Correspondence: A. Starr, Department of Neurology, University of California, Irvine, CA 92717, U.S.A. 2~ MATERIALS AND METHODS eyelids of the left eve were kept opell i~ ~i wife k~(,!~ and a pupillometer positioned m tronl ~,~ the e~c t~ Surgi~'al preparation measure pupillary dilation. The pupithmletcr, de- Four female cats weighing from 3.3 to 4.3 kg were scribed elsewhere ~, measured the ;_ltll()tti~ of light re- used in this study. Otoscopic examination verified flected from the iris. To prevent drying ni the ext, that each animal was free from ear lice and that the thin layer ofIerramycm eve ointment x~ applied tympanum was clearly visible. Surgical preparation Auditory stimuli consisted of I kliz told 4 kHz occurred in two stages. Initially under general anes- tones, 50 ms in duration, with a rise tim~:~ o( 5 ms and thesia a headholder was implanted, and a stainless an intensity of 65 dB SPI~. Stimuli were delivered steel screw recording electrode placed either 1 or 11 through Beyer earphones coupled to the cat's left ear mm behind the bregma to serve as a fixed control re- bv a hollow plastic tube. Behavioral reinforcement cording site. After the development of a P3011 com- was produced by a constant current eleclrical stimu- ponent during training a second surgery was per- lus administered to the tail 7t)(I ms after onset of the 1 formed. The animals were re-anesthetized and from kHz tone. The electrical stimulus consisted of a 300 one to five cannulas were implanted in the right side ms train of 15 pulses (2 mA, 2 ms) delivered through of the skull. The cannulas were constructed from 14 a pair of ring electrodes placed 2 cm apart on a gauge stainless steel tubing. The dura was not pen- shaved portion of the cat's tail. etrated in this procedure, and sterile bone wax was packed into the cannulas to reduce refection. Fig. I Behavioral paradigm shows the placement of cannulas relative to the corti- A variation of the 'oddball paradigm" employed m cal surface. All surgery was performed under sodium human P300 studies was utilized (Fig. 2A). Cats pentobarbital anesthesia (40 mg/kg). Cats were al- were presented with a random series of two tones, a lowed at least one week to recover before training or 'frequent" 4 kHz stimulus and a 'rare" l kHz stimulus electrophysiological data recording connnenccd. at two-second intervals. The electrical stimulus to the tail was administered 700 ms after onset of the 4 kHz General procedures tone. This procedure led to a conditioning of a pupil- The cats were paralyzed with galleminc triethio- lary dilation, which began about 300 ms after onset of dide (10 mg/kg), intubated, and artificially respi- the 4 kHz tone. When conditioning is established, the rated, and then supported on a piece of foam rubber. rare stimulus elicits a positive potential at the vertex Expired carbon dioxide was maintained near 4%. similar to the human P3007,~°. The pupil response Body temperature was monitored by a rectal ther- served as a 'behavioral' measure of the animal's con- mometer and maintained by a circulating water heat- ditioning to the Fare 4 kHz stimulus. ing pad, Experiments were carried out in a double- Training began with an habituation phase during walled sound attenuating chamber with the cat's which no shock was employed. During habituation head held in place by the implanted headholder. The approximately 4(10 stimuli, l(lC/c of which were 'rare'~ were presented. Usually at the end of such a stimulus series, no conditioned pupil response was apparent to either stimulus as well as no late positive skull poten- tials. In all cases conditioning was not begun until the averaged pupil response showed stimulus related di- lation to be absent. During conditioning stimuli were presented in blocks of 400 and within three or four such blocks the conditioned pupillary response and P300 attained maximum values. Fig. 2 shows the de- velopment of the P300 recorded at the skull (B) and the pupillary dilation response (C) m one of the cats. The uppermost records on each side represent the Fig. 1. Location of implanted cannulas relative to the cortical surface. MG, marginal gyrus: SSG. suprasylvian gyrus. averaged event-related potential and pupillary dila- 29 A. The paradigm was controlled by a PDP 11/40 com- puter including randomization of the signal se- TAIL SHOCK quence, tone duration, and electric stimulus deliv- RARE TONE I ery. FREQUENT TONE I IIII Neural recording ill I,L, Intracranial electrodes were constructed from 0 1 2 3 ...........5 6 7 8 9 ,0 .....I1 12 I , .....14 15 16 Seconds 0.005 inch diameter stainless steel wire insulated with . SKULL RECORDS C. PUPIL RESPONSES epoxylite. The insulation was removed from the ter- .... HABITUATION minal 200-300 um of each electrode, lntracranial electrodes were held in stereotaxic carriers and ad- i CONDITIONING vanced into the brain through implanted cannulae. The potential recorded from a skull electrode (steel screw) near the vertex was monitored during intra- cranial electrode advancement. Generally no more than two intracranial electrodes were simultaneously employed. Electrode recordings were obtained rela- tive to an indifferent needle electrode in the back of the neck. A ground electrode was located approxi- L L J I I I I I I I 1 200 400 600 O 200 400 Ca00 mately 1 inch posterior to the indifferent electrode. MllhSeconds M~ h seconds Brain potentials were amplified 1000 times with a Fig. 2. Diagram of classical conditioning paradigm (A) used in this study. A random series of 'frequent' 4 kHz and 'rare' 1 kHz band pass of 0.1 to 300 Hz (3 dB points, 6 dB/octave tones were presented at 2-second intervals.
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