Proc. Natl. Acad. Sci. USA Vol. 93, pp. 1654-1658, February 1996 Neurobiology Learning and recall of form discriminations during reversible cooling deactivation of ventral-posterior suprasylvian cortex in the cat (memory/object and pattern discriminations/area 20/inferotemporal cortex/monkey) STEPHEN G. LOMBER*t, BERTRAM R. PAYNE*, AND PAUL CORNWELL*t *Laboratory for Visual Perception and Cognition, Department of Anatomy and Neurobiology, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118; and tDepartment of Psychology, 130 Moore Building, The Pennsylvania State University, University Park, PA 16802 Communicated by Irving T. Diamond, Duke University Medical Center, Durham, NC, October 31, 1995 ABSTRACT Extrastriate visual cortex of the ventral- posterior suprasylvian gyrus and the fusiform gyrus. The cats' posterior suprasylvian gyrus (vPS cortex) of freely behaving ability to discriminate pattern or object pairs was tested while cats was reversibly deactivated with cooling to determine its cortex was warm (active) and cool (deactivated). We examined role in performance on a battery of simple or masked two- discrimination performance on four tasks: (i) highly familiar dimensional pattern discriminations, and three-dimensional simple two-dimensional patterns; (ii) highly familiar masked or object discriminations. Deactivation of vPS cortex by cooling partially occluded patterns; (iii) highly familiar three- profoundly impaired the ability of the cats to recall the dimensional objects; and (iv) recently learned or novel objects. difference between all previously learned pattern and object Apparatus and Method. A two-choice Pennsylvania General discriminations. However, the cats' ability to learn or relearn Testing Apparatus (PGTA) was used for all discrimination pattern and object discriminations while vPS was deactivated training and testing (7, 8). Detailed procedures for apparatus depended upon the nature ofthe pattern or object and the cats' acclimation and training are described elsewhere (7). Patterns prior level of exposure to them. During cooling of vPS cortex, were displayed on video monitors in each goal compartment. the cats could neither learn the novel object discriminations For object discriminations, the video displays were removed, nor relearn a highly familiar masked or partially occluded and objects were centrally located in the distal half of each goal pattern discrimination, although they could relearn both the compartment. A discrimination trial began with the animal in highly familiar object and simple pattern discriminations. the start box and the raising of an opaque door for the cat to These cooling-induced deficits resemble those induced by view the discriminanda through a transparent door. Two cooling of the topologically equivalent inferotemporal cortex seconds later, the transparent door was raised and the cat of monkeys and provides evidence that the equivalent regions entered the decision area. The cat was deemed to have made contribute to visual processing in similar ways. a decision when both front paws were set down across a line separating the decision area from the goal compartments. For In mammals, both the learning and recall of pattern and object responding to the positive stimulus, cats were rewarded with discriminations depends upon cerebral cortex. In monkeys, the soft commercial cat food, which they found behind a lip above ability to discriminate between pairs of patterns or objects has the video monitor or behind the object. been localized and depends upon inferotemporal (IT) cortex Training. Initial training was done binocularly and the cats (1). In cats, the topologically equivalent cortex (2) comprises were taught to discriminate between a solid black "I" and "O"U the ventral half of the posterior suprasylvian gyrus (vPS object, simple patterns (outline I and 0), and masked patterns cortex), and it is known that this region contributes to the (outline I and 0 masked by multiple intersecting diagonal lines); learning of some pattern discriminations (3-5), but no previ- to criterion levels of performance (92%; 23 correct responses out ous investigation has identified any clear contribution of vPS of 25 consecutive trials). After reaching criterion, the cats con- cortex to the learning or recall of objects or masked patterns. tinued to be trained on each I vs. 0 discrimination for an These shortfalls in our knowledge of vPS cortex have made it additional 5000 trials to ensure the cats were highly familiar with difficult to determine whether cat vPS cortex has more than the discriminations. For discriminations designed to test learning a superficial functional similarity to monkey IT cortex (2). of new discriminations, the cats were initially trained to discrim- We attempted to clarify this relationship by examining the inate multiple pairs ofjunk objects (>20) prior to exposure to the abilities of cats to learn and recall a battery of pattern and tested object pairs. Recall of these object discriminations was object discriminations while the vPS cortex was deactivated examined 4-18 hr later in a single block of 25 trials. by cooling. Surgical Procedures. Following initial training, the cats underwent three surgical procedures to: (i) section the optic MATERIALS AND METHODS chiasm in the midline by a transoral approach to allow visual signals to be directed to one hemisphere when the contralat- Two laboratory-reared cats [Toonces (Cat T) and Sid (Cat Sd)] eral eye was occluded; (ii) transect the visual fibers in the were studied and treated in accordance with the National corpus callosum (9) to eliminate possible direct interactions Institutes of Health Guide for the Care and Use of Laboratory between visual cortices in the two hemispheres (10); and (iii) Animals (no. 86-23). The cats were trained on a series of install subdural cortical cooling probes over vPS cortex of the two-choice pattern- or object-discriminations prior to midline right hemisphere. All procedures were performed by antiseptic sections of the optic chiasm and the caudal two-thirds of the methods and with the cats fully anesthetized with sodium corpus callosum. Cooling probes (6) were permanently im- pentobarbital (40 mg/kg i.p. and i.v. as necessary). The planted in contact with cortex of the ventral half of the right completeness of the optic chiasm section was verified following The publication costs of this article were defrayed in part by page charge Abbreviations: vPS cortex, ventral-posterior suprasylvian gyrus; IT, payment. This article must therefore be hereby marked "advertisement" in inferotemporal. accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 1654 Downloaded by guest on September 29, 2021 Neurobiology: Lomber et al. Proc. Natl. Acad. Sci. USA 93 (1996) 1655 surgery by the complete loss of the peripheral visual fields in v psss a visual perimetry test. Cooling Probes. Loops of 23-gauge hypodermic tubing were shaped to conform to the shape of vPS cortex and the fusiform 5. -A gyrus. Cooling was effected by pumping cold methanol through the hypodermic tubing. Temperature of the cooling probe was monitored continuously via a thermocouple at- tached to the probe and was kept constant (±+1C) by adjusting the methanol flow rate. Following probe implantation, the cats wore a harness during testing and were loosely tethered to an overhead bar. The tether supported the cooling tubes and temperature monitoring wire and was long enough to afford the animal complete freedom of movement within the appa- ratus. Testing. The cats' capacity to recall the highly familiar patterns and objects was tested while the cortex either was at normal body temperature and active or was cooled and FIG. 1. Horizontal section through vPS cortex stained for Nissl deactivated. Testing consisted of a single 25-trial block in each substance. Measurement sites (arrowheads) are identified and tem- of three to six individual sessions. In the next series, which peratures are indicated. The probe was cooled to 3°C. The black line continued for the next 4 days, the cat's capacity to relearn the through cortex estimates the position of the 20°C thermocline and same highly familiar pattern or object discriminations was separates the deactivated regions close to the pial surface from the tested until either criterion performance was reached or active regions either close to white matter or some distance away from 100-150 trials were performed on a given day. During this the cooled region. Two small nicks in layer I resulted during tissue testing, the vPS probe was cooled to 3 ± PC. On day 5, the cats' processing. A, anterior; H, hippocampal formation; L, lateral; psss, capacity to relearn the discrimination was tested with vPS posterior suprasylvian sulcus; T, tentorial surface; V, lateral ventricle. cortex at normal body temperature and active. In the final (Bar = 3 mm.) series, the cats' capacity to learn novel object discriminations conduction, and there were certainly no direct effects of was also tested while the vPS cortex was cooled. Since the cats cooling on neural processing in hippocampus and nearby showed no evidence of being able to learn an object discrim- structures. ination with vPS cortex cooled, they were then trained with Behavior. Detailed data on recall and (re)learning of various cortex warm. Subsequently, their capacity to recall the same form discriminations from Cats T and Sd are presented in Fig. 3. discrimination was tested 4-18 hr later in two blocks of 25 Recall. vPS cortex is critical for the recall of both trials. During the first block of trials vPS cortex was cooled and highly deactivated, familiar and recently learned form discriminations. In each cat, and in the second block, vPS cortex was warm. and for both pattern and object discriminations, cooling of the Final Procedures. At the conclusion of behavioral testing, vPS cortex completely the cats were anesthetized (sodium pentobarbital, 40 mg/kg, blocked the cats' capacity to recall the i.p.), and temperatures in cortex were measured with micro- discriminations (column C in i of Fig.