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Reflections on the Past Two Decades of Neuroscience VIEWPOINT medium of conceptual space is: how do we combine these twin paths to understand Reflections on the past two decades the transmission of representations in the network of the brain? Although answering of neuroscience that question will surely build on the prior paradigms, neither seems equipped to Danielle S. Bassett , Kathleen E. Cullen , Simon B. Eickhoff , provide a complete solution; the former offers the dots within, whereas the latter Martha J. Farah , Yukiko Goda , Patrick Haggard , Hailan Hu , offers the lines between. Yet obtaining such Yasmin L. Hurd , Sheena A. Josselyn , Baljit S. Khakh , Jürgen A. Knoblich , a solution is important for deciphering the Panayiota Poirazi , Russell A. Poldrack , Marco Prinz , Pieter R. Roelfsema , mechanism of the brain’s fundamental goal: Tara L. Spires-Jones , Mriganka Sur and Hiroki R. Ueda information processing. The efforts towards such a solution that I find particularly Abstract | The first issue of Nature Reviews Neuroscience was published 20 years promising are those that move beyond ago, in 2000. To mark this anniversary, in this Viewpoint article we asked a selection descriptive characterization or correlative of researchers from across the field who have authored pieces published in the approaches, and towards theory; that is, journal in recent years for their thoughts on notable and interesting developments theory instantiated in an interpretable and generalizable mathematical model in neuroscience, and particularly in their areas of the field, over the past two that encodes a conceptual principle, and decades. They also provide some thoughts on current lines of research and theory as supported by (but not composed questions that excite them. of) computational and machine-learning approaches applied to data shared publicly in the spirit of open science. Progress along Broadly, how has the field of neuroscience and a growing (rather than diminishing) this tack will require more interdisciplinary changed over the past two decades, and undercitation of women in the reference lists graduate training programmes that provide what do you regard as the most notable or of neuroscience journal articles in the past equal depth in theory and experiment. interesting developments within your area of the 20 years. Each of us as citizens of science field over that period? What do you think are can choose to own and mould our culture Kathleen E. Cullen. Traditionally, the field the most interesting, big-picture questions being to realize a more equitable future. of neuroscience has asked the question: how asked in your area currently? Which lines of As a practice in the acquisition and is sensory input (afference) transformed research in your area of neuroscience are you curation of knowledge, neuroscience has into motor output (efference) to generate particularly excited about? expanded upon prior paradigms. In human appropriate behaviour? This conceptual neuroscience, I have been particularly struck framework — initially made popular by Danielle S. Bassett. Science is a culture by a concerted effort to move beyond the Sherrington — has long served as a common as much as it is a practice in the acquisition activation studies that were characteristic of foundation for systems neuroscientists. and curation of knowledge. As time passes, the brain-mapping era. Leading from that A fundamental development over the past the field changes its culture and practice. point in scholarly space, two particularly two decades, however, has been a collective As a culture, neuroscience is now composed pioneering paths of formal study extend: realization that it is necessary to reverse this of a more diverse group of scientists, along that of neural representations and that of traditional perspective. A series of recent the dimensions of sex, gender, sexual network systems. The former considers studies has established that motor signals orientation, race, ethnicity and disability. the pattern of activity across neural units profoundly influence sensory processing With the creation of anneslist (anneslist. that encodes an object, concept or state of during voluntary behaviour. In particular, net), Women in Neuroscience Repository information. The latter considers the pattern experiments across sensory systems have (winrepo.org) and BiasWatchNeuro of connections between neural units that can provided circuit-level insight into how (biaswatchneuro.com), there exist resources support the transmission of information and motor-related inputs to sensory areas to increase awareness of the work of women the modulation of network state in a manner selectively cancel self-generated sensory scientists, and to encourage a greater balance that alters the repertoire of computations inputs. This neural strategy underlies an in the speaker line-ups of conferences and accessible to a given neural population. essential property of the brain, namely its symposia. Yet explicit bias exists now as it The twin paths of representation and ability to distinguish externally applied did in 2006 when transgender Professor transmission move beyond the mapping of a (exafferent) from self-generated (reafferent) Ben A. Barres (Stanford University) wrote country’s borders, to record a city’s statistics sensory inputs. For instance, work by my his commentary for Nature entitled ‘Does and the transportation networks along group has established that neurons at the Gender Matter?’ And implicit bias is perhaps which traffic flows. first central stage of vestibular processing even more pervasive, as reflected in peer To me, the question that creates giant preferentially encode sensory exafference. review, paper acceptance rates, grant funding resonance when dropped into the liquid Moreover, researchers studying other NATURE REVIEWS | NEUROSCIENCE VIEWPOINT sensory pathways (for example, visual, based on motor-related inputs is vital for and cognitive processing that is central to somatosensory and auditory) have both perceptual stability and accurate our subjective awareness of initiating and shown suppression of reafferent sensory motor control. This computational strategy controlling our own volitional actions in the information by motor-related inputs also provides the flexibility required for world (that is, our sense of agency). In this at higher levels of sensory processing, fine-tuning and updating relationships context, a fundamental question logically including in the cortex. between motor signals and resultant arises: how exactly does the brain actually Indeed, much of the sensory input sensory feedback in order to compensate predict the sensory consequences of our that we experience in our everyday lives for changes to our body or the environment. actions in a dynamically changing world? is reafferent as it is generated by our own Furthermore, the ability to distinguish Two particularly exciting lines of research behaviour. The brain’s ability to predict between sensory exafference and reafference are currently addressing this question. the sensory consequences of our actions is a hallmark of higher-level perceptual First, emerging technologies including The contributors Danielle S. Bassett is the J. Peter Skirkanich Professor at the University role of astrocytes in neural circuits. The Khakh laboratory develops of Pennsylvania, Departments of Bioengineering, Electrical and Systems and uses novel genetic and optical methods to explore glial biology Engineering, Physics and Astronomy, Neurology, and Psychiatry. Her in vivo. expertise centres on the architecture, function, design and control of Jürgen A. Knoblich is Director of the Institute of Molecular Biotechnology complex systems, with a particular focus on large-scale neural systems of the Austrian Academy of Sciences in Vienna. He is a developmental in humans. neuroscientist studying human brain development and psychiatric Kathleen E. Cullen is a professor of biomedical engineering at the Johns disorders. Researchers in his group have developed a method for growing Hopkins University School of Medicine. She holds joint appointments human brain tissue in the laboratory. They can recapitulate human in neuroscience and in otolaryngology. Her expertise in systems and embryonic brain development during the first trimester and analyse the computational neuroscience uses state-of-the-art methodologies that developmental defects leading to neurological disorders. manipulate and monitor neural circuits to understand the neural Panayiota Poirazi is a Research Director at the Foundation for Research computations that predict the consequences of natural self-motion and and Technology-Hellas (FORTH) in Heraklion, Crete, Greece. She uses the implications for perception and action. mathematical and computational techniques to develop experimentally Simon B. Eickhoff is a neuroimaging researcher at the Heinrich-Heine constrained models of single neurons and neuronal networks, aiming at University Düsseldorf and the Forschungszentrum Jülich. At the interface inferring the contributions of dendritic computations to complex brain between neuroanatomy, data science and medicine, his work combines functions. brain mapping, modelling of inter-individual differences and brain– Russell A. Poldrack is the Albert Ray Lang Professor in the Department of phenotype relationships as well as machine learning for single subject Psychology and Professor (by courtesy) of Computer Science at Stanford prediction of behavioural traits and precision medicine. University, and Director of the Stanford
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