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Organization of Ocular Dominance and Orientation Columns in the Striate Cortex of Neonatal Macaque Monkeys

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Organization of Ocular Dominance and Orientation Columns in the Striate Cortex of Neonatal Macaque Monkeys Visual Neuroscience (1995), 12, 589-603. Printed in the USA. Copyright © 1995 Cambridge University Press 0952-5238/95 $11.00 + .10 Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys GARY BLASDEL,1'2 KLAUS OBERMAYER,3-4 AND LYNNE KIORPES5 'Department of Physiology, University of Calgary, Calgary Alberta, Canada T2N-1N4 2Department of Neurobiology, Harvard Medical School, Boston 3The Salk Institute, La Jolla "The Rockefeller University, New York 'Center for Neural Science, New York University, New York (RECEIVED May 13, 1994; ACCEPTED November 30, 1994) Abstract Previous work has shown that small, stimulus-dependent changes in light absorption can be used to monitor cortical activity, and to provide detailed maps of ocular dominance and optimal stimulus orientation in the striate cortex of adult macaque monkeys (Blasdel & Salama, 1986; Ts'o et al., 1990). We now extend this approach to infant animals, in which we find many of the organizational features described previously in adults, including patch-like linear zones, singularities, and fractures (Blasdel, 19926), in animals as young as 3| weeks of age. Indeed, the similarities between infant and adult patterns are more compelling than expected. Patterns of ocular dominance and orientation, for example, show many of the correlations described previously in adults, including a tendency for orientation specificity to decrease in the centers of ocular dominance columns, and for iso-orientation contours to cross the borders of ocular dominance columns at angles of 90 deg. In spite of these similarities, there are differences, one of which entails the strength of ocular dominance signals, which appear weaker in the younger animals and which increase steadily with age. Another, more striking, difference concerns the widths of ocular dominance columns, which increase by 20% during the first 3 months of life. Since the cortical surface area increases by a comparable amount, during the same time, this 20% expansion implies that growth occurs anisotropically, perpendicular to the ocular dominance columns, as the cortical surface expands. Since the observed patterns of orientation preference expand more slowly, at approximately half this rate, these results also imply that ocular dominance and orientation patterns change their relationship, and may even drift past one another, as young animals mature. Keywords: Development, Primate striate cortex, Ocular dominance, Orientation selectivity Introduction appear to be organized in slab-shaped regions, 0.25-0.5 mm wide, that run vertically between pia and white matter, that lie Neurophysiological studies have shown that most neurons in in register with bands of afferents from the appropriate eye in striate cortex are binocular and selective for orientation (Hubel layer 4c, and that interdigitate with slabs dominated by the other &Wiesel, 1962, 1968, 1972, 1974a,b). Their binocularity is fur- eye (Hubel & Wiesel, 1972; LeVay et al., 1975; Hubel & Wiesel, ther characterized by a preference for one eye, referred to as 1977). Preferences for orientation also appear to be organized "ocular dominance," and their preference for orientation is fur- in slabs, but ones that are much narrower and shorter in length. ther characterized by a degree of selectivity, which is frequently The main reason these slabs are shorter is that they converge referred to as "orientation selectivity" or "orientation tuning." periodically in the centers of ocular dominance columns, at As numerous studies have shown, these response properties are points, or singularities, which take on the appearance of not strewn about randomly, but are highly organized across the "rosettes" or "pinwheels" when preferences for different ori- cortical surface. Cells preferring a particular eye, for example, entations are illustrated in color, as they are in Fig. la (Blasdel & Salama, 1986; Blasdel, 19896, 1992; Ts'o et al., 1990; Bon- hoeffer & Grinvald, 1991). Because most orientation slabs Reprint requests to: Gary Blasdel, Department of Neurobiology, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, extend between singularities in adjacent ocular dominance col- USA. umns, they tend to cross their borders at right angles (Obermayer 589 Downloaded from https://www.cambridge.org/core. NYU Medical Center: Ehrman Medical Library, on 23 Feb 2018 at 18:59:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0952523800008476 590 C. Blasdel, K. Obermayer, and L. Kiorpes et al., 1992a; Blasdel, 19926; Bartfeld & Grinvald, 1992; Ober- orientation signals, in young animals, as well as a tendency for mayer & Blasdel, 1993), as illustrated in Fig. lc. ocular dominance bands to lie closer together than one might We were interested in looking at how these organizations expect from their adult spacing corrected for expected rates of emerge in young animals. Previous work had indicated that vari- postnatal growth (Purves & LaMantia, 1993). Some of these ations in orientation preference and ocular dominance are results have been presented previously in abstract or seminar present at birth (Wiesel & Hubel, 1974). But the fact that bands form (Kiorpes & Blasdel, 1987; Blasdel, 1989; Obermayer et al., of afferents are not fully segregated in layer 4c until 8-10 weeks 1994). of age, makes it unlikely that organizations associated with them (e.g. ocular dominance and orientation) can mature before this time. We began investigating these issues by using optical imag- Materials and methods ing techniques to explore the organizations of ocular dominance and orientation at discrete ages during the first 14 weeks of life. In so doing, we found that patterns of ocular dominance and Infant monkeys orientation are both present in all animals (as young as 3| These studies were conducted on four Macaca nemestrina (BN- weeks of age), with adult characteristics and interactions (e.g. 5.5, BN-7.5, BN-9, and BN-14) and one Macaca fascicularis linear zones, fractures, singularities, saddle points, and instances (BF-3.5) infants. The Macacae nemestrina were all born in the of orientation slabs crossing ocular dominance borders at right animal vivarium at the University of Calgary, where they were angles) clearly evident at all times. We also observed a tendency reared by their mothers. BF-3.5 was born at the New England for ocular dominance signals to appear weaker, in relation to Regional Primate Center and reared by hand. At the time of linear zone a) singularity saddle point fracture linear zone b) singularity saddle point fracture C) L R L Downloaded from https://www.cambridge.org/core. NYU Medical Center: Ehrman Medical Library, on 23 Feb 2018 at 18:59:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0952523800008476 Development of dominance and orientation preference 591 study, the mother was tranquilized with an intramuscular injec- catheter for the infusion of electrolytes and drugs. It was ven- tion of ketamine/xylazine, to facilitate removal of the infant, tilated with a 2:1 mixture of nitrous oxide and oxygen, and anes- which was then anesthetized with halothane (0.5-1.5%) in thesia was switched gradually to Pentothal (0.1-1.0 mg/kg/h, nitrous oxide/oxygen, and prepared for neurophysiological and i.v.), as the residual halothane was expired. optical recording. Each animal was placed on a heated waterbed with its head Experiments were limited to 18-h duration, after which the in a stereotaxic frame. The scalp was then reflected and a tre- animals were either allowed to recover and return to their moth- phine or dental drill used to bore a 25-mm hole in the cranium ers, or killed with an overdose of Pentobarbitol and perfused overlying the opercular cortex, just behind the lunate sulcus, through the heart with 4% paraformaldehyde in 0.1 M phos- as close to the midline as possible. In some cases, especially for phate buffer. Animals that were allowed to recover were first the very young infants whose cranial sutures were immature, weaned of drugs. After it became apparent they could breathe the cranial bones were additionally secured by an acrylic cap on their own, they were given supplemental doses of pyrido- constructed from a thin layer of Grip Cement. After this, a stigmine, to reverse any residual effects of curariform drugs, stainless-steel chamber suitable for either microelectrode or and methamphetamine, to counteract the residual effects of optical recordings was inserted and cemented in place. For the thiopental sodium administered during the experiment. After electrode recordings, this chamber was sealed by an O-ring sup- animals had recovered fully, and demonstrated their ability to porting a large glass disk that was pressed against it by a micro- vocalize, they were returned to their mothers who on some, but manipulator. The glass contained a guide tube that allowed an not all, occasions accepted them. Infants that were not accepted electrode to be inserted and positioned anywhere on the corti- were reared in an incubator and nursed on a 1:1 mixture of cal surface under visual guidance. For the optical recordings a Similac and water until the conclusion of the experiment, at threaded stainless-steel plug, equipped with an 18-mm glass win- which time they were killed with an overdose of barbiturate and dow, was inserted into the chamber and adjusted until the glass perfused as outlined above. rested a millimeter above the cortical surface. A minimum sep- aration of 0.5-1.0 mm was maintained between glass and cor- tex to allow the dye solution (NK2367, 0.1% in saline) to Preparation circulate. The results in this article are based on optical and single-unit After all surgical procedures had been completed the animal recordings from five infant macaque monkeys, that ranged in was paralyzed partially with Vecuronium bromide or Tubocu- age between 3j and 14 weeks.
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