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Neuroimaging: Perception at the Brain's Core

2006; Elsevier BV; Volume: 16; Issue: 3 Linguagem: Inglês

10.1016/j.cub.2006.01.026

1879-0445

David A. Leopold, Alexander Maier,

Visual perception and processing mechanisms

Two new functional imaging studies have shown that activity in the lateral geniculate nucleus of the thalamus strongly reflects perceptual dominance during binocular rivalry, raising new questions about how subjective percepts arise in the brain. Two new functional imaging studies have shown that activity in the lateral geniculate nucleus of the thalamus strongly reflects perceptual dominance during binocular rivalry, raising new questions about how subjective percepts arise in the brain. How can activity in the brain possibly give rise to our subjective experience? This question can be traced back at least to René Descartes, the father of modern philosophy who lived in the 17th century. In his Treatise on Man [1Descartes R. (1662). De homine, Leyden.Google Scholar], Descartes hypothesized that a percept arises when a sensory stimulus impresses upon the pineal gland, which communicates directly with the soul (Figure 1A, soul not shown). In explaining his choice of the pineal gland, the only unpaired structure in the brain he could identify, he appealed to the unity of perception: “Since we see only one thing with two eyes, … it must necessarily be the case that the impressions which enter by the two eyes…unite with each other in some part of the body before being considered by the soul” [2Lokhorst, G.-J. (2005). Descartes and the Pineal Gland. The Stanford Encyclopedia of Philosophy. (Fall, 2005 Edition, ed. Zalta, E.N.). http://plato.stanford.edu/archives/fall2005/entries/pineal-gland/.Google Scholar]. In modern times, Descartes' brain theory is irreconcilable with the known physiology of the brain, and is often disparaged among neuroscientists as the prototype of unscientific mind–body dualism. Yet we must admit that his original questions linger. How does the brain create unity in our perception despite paired sensory organs? And, more generally, how could any biological circuitry create a subjective percept? In recent years, a theoretical framework has arisen to study the scientific basis of conscious perception [3Koch C. The Quest for Consciousness: A Neurobiological Approach. Roberts and Company, Englewood, Colorado2003Google Scholar]. Experimental techniques ranging from single-cell recordings in laboratory animals to functional magnetic resonance imaging (fMRI) in humans have sought to identify specific neural correlates of our visual experience. Typically, such experiments involve tracking activity in the brain under conditions where perception wavers despite an unchanging sensory stimulus. Particularly prominent in recent years has been the study of binocular rivalry, where paired, but conflicting, monocular visual patterns are presented simultaneously to the two eyes [4Blake R. Logothetis N.K. Visual competition.Nat. Rev. Neurosci. 2002; 3: 13-21Crossref PubMed Scopus (1005) Google Scholar]. Under such conditions, perception impressively reverses every few seconds between the left- and right-eye's views, raising questions about what sort of changes in the brain might accompany this subjective switching. Two recent studies [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar, 6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar] have gained new ground on this important topic by using fMRI to examine a small structure at the core of the brain. Haynes et al. [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar] and Wunderlich et al. [6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar] both examined activity fluctuations in the lateral geniculate nucleus (LGN) during spontaneous perceptual changes in binocular rivalry. And, quite surprisingly, both studies found that activity in the LGN was strongly correlated with the subjects' perception. This result is surprising because the LGN, a portion of the thalamus devoted to vision (Figure 1B), is seldom considered to be directly involved in perception. It is a laminated structure, where information from the two retinas remains strictly segregated, with each internal layer consisting of a topographic map of the entire visual hemifield. Yet, while most would consider the LGN to be simply passing basic visual information along to the cerebral cortex, there are some notable mysteries about this structure. For example, it is well-known that the LGN receives considerable highly organized projections, directly and indirectly, from the cortex. While many have speculated on the functional significance of this so-called corticofugal input, including its role in binocular rivalry [7Singer W. Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system.Physiol. Rev. 1977; 57: 386-420PubMed Google Scholar], the function of these connections remains a mystery [8Sherman S.M. Guillery R.W. Exploring the thalamus. Academic Press, London, UK2001Google Scholar]. In demonstrating strong perceptual modulation during rivalry, both recent studies represent a potential step forward in understanding how cortical and subcortical structures might interact in the generation and maintenance of a subjective percept. The approaches of the two groups were somewhat different, and in a sense complementary. Wunderlich et al. [6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar] used a previously applied technique [9Polonsky A. Blake R. Braun J. Heeger D.J. Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry.Nat. Neurosci. 2000; 3: 1153-1159Crossref PubMed Scopus (425) Google Scholar] that exploits the increased responses of neurons to high contrast patterns compared to low contrast ones. In short, they created binocular rivalry between a faint stimulus (to one eye) and a high-contrast one (to the other) and observed the activity in the LGN as the two stimuli alternately dominated the observers' perception. Remarkably, they found that the activity fluctuations were roughly as large during subjective perceptual changes as they were when the high and low contrast patterns were physically alternated on the screen [6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar]. Haynes et al. [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar] used a slightly different technique that allowed them to go one step further. Applying high resolution imaging techniques, they first identified the monocular preferences of voxels throughout the LGN — biases thought to arise due to differential contributions of the left-eye and right-eye layers within each voxel. They next found that by monitoring these voxels of known ocular bias during fMRI testing, they were able to predict with great accuracy which eye was phenomenally dominant at each point in time [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar] (Figure 2). One interpretation of these findings, perhaps the simplest, would be that information from the non-dominant eye is blocked at this relay nucleus, and thus never makes it to the cortex. Perception would thus represent the only information that passed this checkpoint on to the rest of the brain. This notion is largely consistent with several previous human fMRI studies investigating this phenomenon [9Polonsky A. Blake R. Braun J. Heeger D.J. Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry.Nat. Neurosci. 2000; 3: 1153-1159Crossref PubMed Scopus (425) Google Scholar, 10Tong F. Engel S.A. Interocular rivalry revealed in the human cortical blind-spot representation.Nature. 2001; 411: 195-199Crossref PubMed Scopus (358) Google Scholar, 11Lee S.H. Blake R. Heeger D.J. Traveling waves of activity in primary visual cortex during binocular rivalry.Nat. Neurosci. 2005; 8: 22-23Crossref PubMed Scopus (194) Google Scholar]. Yet this interpretation, however alluring, cannot be correct, as there is equally compelling evidence to the contrary. Single-unit recordings in the LGN of monkeys during binocular rivalry did not find evidence of state-dependent activity changes [12Lehky S.R. Maunsell J.H. No binocular rivalry in the LGN of alert macaque monkeys.Vision Res. 1996; 36: 1225-1234Crossref PubMed Scopus (69) Google Scholar]. Furthermore, recordings in the primary visual cortex, which receives the major output of the LGN, showed only modest perceptual modulation during binocular rivalry [13Leopold D.A. Logothetis N.K. Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry.Nature. 1996; 379: 549-553Crossref PubMed Scopus (701) Google Scholar, 14Gail A. Brinksmeyer H.J. Eckhorn R. Perception-related Modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry.Cereb. Cortex. 2004; 14: 300-313Crossref PubMed Scopus (118) Google Scholar, 15Fries P. Roelfsema P.R. Engel A.K. Konig P. Singer W. Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry.Proc. Natl. Acad. Sci. USA. 1997; 94: 12699-12704Crossref PubMed Scopus (394) Google Scholar]. In addition, psychophysical experiments, while affirming that ocular segregation is a key feature of binocular rivalry [16Blake R. Westendorf D.H. Overton R. What is suppressed during binocular rivalry?.Perception. 1980; 9: 223-231Crossref PubMed Scopus (151) Google Scholar], are incompatible with an early monocular blockade at the stage of the LGN [17Blake R. Fox R. Adaptation to invisible gratings and the site of binocular rivalry suppression.Nature. 1974; 249: 488-490Crossref PubMed Scopus (144) Google Scholar, 18Logothetis N.K. Leopold D.A. Sheinberg D.L. What is rivalling during binocular rivalry?.Nature. 1996; 380: 621-624Crossref PubMed Scopus (425) Google Scholar]. But if perceptual suppression does not take this form, then how can the present results be explained? One of the most intriguing aspects of the new experiments [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar, 6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar] is that they, more than previous studies, force us to rethink how different techniques might provide different perspectives on neural correlates of perception. For one, they add the strongest evidence to date that imaging techniques can detect modulation that is, for reasons that we do not yet understand, largely absent in the spiking of individual neurons [4Blake R. Logothetis N.K. Visual competition.Nat. Rev. Neurosci. 2002; 3: 13-21Crossref PubMed Scopus (1005) Google Scholar, 19Posner M.I. Gilbert C.D. Attention and primary visual cortex.Proc. Natl. Acad. Sci. USA. 1999; 96: 2585-2587Crossref PubMed Scopus (147) Google Scholar]. Recent work in monkeys has emphasized the contribution of non-spiking activity to the fMRI signal, which may account for some of the difference [20Logothetis N.K. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2002; 357: 1003-1037Crossref PubMed Scopus (680) Google Scholar]. Furthermore, the volumetric nature of the fMRI measurement is fundamentally different from the monitoring of electrical discharges from single, localizable neurons. Each voxel contains thousands to millions of neural elements, whose activity at each point in time is condensed down to a single number measured through the vascular response. To wit, using the fluctuation of fMRI intensity to make inferences about complex neural processes within a voxel might be similar to using the flow through the main plumbing line to understand the activity of people in an office building. While the measured changes will correlate well with some aspects of their behavior, it will be insensitive to others. The notion that electrophysiological and fMRI signals provide complementary information about the perceptual mechanisms in the brain might be taken as good news for scientists struggling to understand the neural basis of rivalry and visual perception in general. The new studies [5Haynes J.D. Deichmann R. Rees G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.Nature. 2005; 438: 496-499Crossref PubMed Scopus (276) Google Scholar, 6Wunderlich K. Schneider K.A. Kastner S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus.Nat. Neurosci. 2005; 8: 1595-1602Crossref PubMed Scopus (227) Google Scholar] are an important step forward because they demonstrate that activity in thalamic relay structures, buried deep within the brain, just a short distance from Descartes' pineal gland, may be critical for understanding how the brain distills a singular perceptual impression from its paired inputs. In the quest for neural correlates of consciousness, these findings may thus foreshadow an increasing appreciation of subcortical structures, acting together with their cortical counterparts, in the generation and maintenance of subjective percepts.