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The 2014 Nobel Prize in Physiology Or Medicine: a Spatial Model for Cognitive Neuroscience

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The 2014 Nobel Prize in Physiology Or Medicine: a Spatial Model for Cognitive Neuroscience Neuron NeuroView The 2014 Nobel Prize in Physiology or Medicine: A Spatial Model for Cognitive Neuroscience Neil Burgess1,* 1Institute of Cognitive Neuroscience and Institute of Neurology, University College London, 17 Queen Square, London WC1N 3AR, UK *Correspondence: [email protected] http://dx.doi.org/10.1016/j.neuron.2014.12.009 Understanding how the cognitive functions of the brain arise from its basic physiological components has been an enticing final frontier in science for thousands of years. The Nobel Prize in Physiology or Medicine 2014 was awarded one half to John O’Keefe, the other half jointly to May-Britt Moser and Edvard I. Moser ‘‘for their discoveries of cells that constitute a positioning system in the brain.’’ This prize recognizes both a paradigm shift in the study of cognitive neuroscience, and some of the amazing insights that have followed from it concerning how the world is represented within the brain. Introduction persuaded of the ‘‘neuro-ethological’’ Two of the most dramatic results of the Early ideas concerning the production of approach in which, faced by a lack of neuro-ethological approach to electro- thought were varied, unconstrained by knowledge about how the brain works, physiology are honored by the Nobel direct experimental data, e.g., Hippo- the primary aim is a broad survey of how Prize: the discoveries of place cells and crates’ theory of cognition depending on the system in question is used during of grid cells. As noted in the Nobel cita- the balance of the four humors (blood, normal behavior. This approach contrasts tion, the properties of these cells, along phlegm, and two types of bile). However, with the principles of more traditional with those of other types of spatial cell, with the advance of technology, the experimental design, with its focus on most notably head direction cells, help importance of electrical signaling in the tightly controlled testing of well-specified to define ‘‘a positioning system in the brain and nervous system slowly became hypotheses, and is well described in the brain.’’ Identification of this specific sys- accepted, from the effects of electrical book written later with Lynn Nadel, his tem is indeed a great achievement in un- stimulation on muscles noted by Luigi friend and colleague from their time at derstanding the link between mind and Galvani in the 18th century, to the cogni- McGill, The Hippocampus as a Cognitive brain. But perhaps even more important tive effects in the human brain noted by Map (O’Keefe and Nadel, 1978). are the general lessons they provide for Wilder Penfield in the 1940s and 50s. O’Keefe also profited from the timely the neural coding of internal cognitive The realization of the importance of neu- advent of modern transistors, allowing constructs, and the neural mechanisms rons (the ‘‘neuron doctrine’’) by Santiago robust differential recording of electrical of learning, representation, and memory. Ramon y Cajal—recipient of the Nobel activity from freely behaving animals, in Prize in 1906 with Camillo Golgi—com- which the large variations in potential Place Cells and Cognitive Maps bined with an appreciation of the role of common to nearby electrodes could be In his first experiments, published with electricity gave rise to the modern field cancelled and the remaining signals Herman Bouma in 1969, O’Keefe re- of electrophysiology as a tool to under- boosted on the animal’s head. Along corded responses in the amygdala of stand brain function. Early successes with other early pioneers such as Jim freely moving cats to ethologically rele- included an understanding of neural re- Ranck, this allowed O’Keefe to introduce vant stimuli (birdsong, mouse shapes, sponses to light in the retina, for which a new paradigm in understanding brain etc.). They found many instances of Granit, Hartline, and Wald received the function—studying neuronal activity in neurons that appeared to be tuned Nobel Prize in 1967, leading to an under- freely behaving animals in response to to represent the presence of specific standing of the feedforward processing naturalistic stimuli or tasks. This paradigm stimuli, when presented, and some that of simple visual stimuli by neurons in the has continued to spread, slowly, over the continued to respond after the stimulus visual system of anaesthetised mammals subsequent decades, notwithstanding was withdrawn. These findings have for which David Hubel and Torsten Wiesel the intrinsic validity of more traditional been echoed recently by neurons in hu- received the Nobel Prize in 1981. approaches in narrowing down potential man amygdala that respond to pictures Amidst these exciting developments in functions as each function becomes of specific animals. the 1960s, John O’Keefe was studying more completely understood. With the Both the amygdala and the neighboring his PhD at McGill University, receiving retrospect of the subsequent 40 years of hippocampus had already been impli- instruction from, among others, Donald progress, the neuro-ethological approach cated in human memory by the finding, Hebb—one of the foremost proponents of electrophysiology in freely behaving at the nearby Montreal Neurological Insti- of looking for direct analogs of learning animals appears to be a crucial ‘‘para- tute founded by Penfield, that bilateral and experience within the brain. As he digm shift’’ for cognitive neuroscience of damage or removal of these structures began his research career, O’Keefe was the kind identified by Thomas Kuhn. and surrounding cortical tissue in the 1120 Neuron 84, December 17, 2014 ª2014 Elsevier Inc. Neuron NeuroView view of the hippocampus as part of a cir- learning and memory in humans. They cuit for emotion, as proposed by James concluded that there must be something Papez. like an innate unitary spatial framework At the invitation of Pat Wall, O’Keefe onto which experience of the world can next moved to University College London be mapped, as foreshadowed by the and into the Department of Anatomy philosopher Immanuel Kant, and that its and Developmental Biology, headed by implementation in the brain should pro- J.Z. Young—another pioneer in relating vide the animal with a ‘‘cognitive map’’ in behavior to neuronal activity (in this the sense argued for by Edward Tolman: case, in the squid). There he began to that is, an abstract and flexible represen- look at the hippocampus in freely moving tation of space allowing novel inferences rodents as they foraged for scattered food (e.g., directions of travel), beyond simple reward. The initial paper, written with representations of specific sensory stim- John Dostrovsky (an MSc student pass- uli, bodily responses, or associations be- ing through the lab on the way to tween them. Within this framework, the becoming a neurologist), describes 8 out place cells were held to represent the of 76 putative neurons responding to the animal’s current environmental location. location of the animal, with other neurons The initial place cell findings aroused responding to arousal, attention, or move- great skepticism, both regarding the ment, or responding in inconsistent or un- basic finding and potential confounds interpretable ways (O’Keefe and Dostrov- such as uncontrolled local sensory stimuli sky, 1971). The responses of many of (e.g., odours), and the bold and highly these cells were consistent with similar abstract interpretation (cognitive maps) early findings by Jim Ranck. as opposed to simpler well-studied forms Perhaps surprisingly, given the appar- of learning such as conditioned re- ently weak initial support, O’Keefe imme- sponses. These justifiable queries were diately recognized these neurons as duly addressed, in sophisticated form. relevant to a classic question in cognitive O’Keefe first showed that the orientation psychology—that of how you represent of the firing locations (‘‘fields’’) could be your own location relative to the envi- controlled by the constellation of distal Figure 1. Examples of the Four Main Types ronment—and christened them ‘‘place cues (O’Keefe and Conway, 1978) and of Spatial Firing Recorded from Neurons in the Hippocampal Formation of Freely cells.’’ In fact, this strong interpretation then that their firing was also robust to Moving Rats was aided by the last seven cells recorded the subsequent removal of the controlling Each example shows firing rate as a function of loca- all being place cells—indicating to cues (O’Keefe and Speakman, 1987). In tion or head direction (left; peak firing rate in Hz O’Keefe that they were the dominant the absence of controlling cues, the orien- above) alongside a plot of the rat’s path within a square box (black line) and the location of the rat response, once the electrodes had tation of the location of a place cell’s firing when an action potential was fired (green dots;right). reached the ‘‘right’’ brain location. Subse- within the environment was unpredictable (A) Place cells, found in areas CA3 and CA1 of the quent experiments revealed that a but remained consistent with those of hippocampus proper, typically fire in a restricted portion of the environment. majority of the principal cells in regions other place cells and with the behavioral (B) Head-direction cells, found in the presubiculum CA1 and CA3 of the hippocampus that choices of the animal. In addition, and deep layers of medial entorhinal cortex, typi- are active in a given environment are O’Keefe laid out his proposal that place- cally fire for a narrow range of allocentric heading place cells, firing action potentials at a cell firing must reflect an internally gener- directions (left). (C) Grid cells, found in medial entorhinal cortex and high rate whenever the animal enters a ated spatial signal based on path integra- pre- and parasubiculum, typically fire in a regular small portion of its environment and re- tion in combination with environmental triangular array of locations.
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