title: Neural constraints on learning.
abstract: Learning, whether motor, sensory or cognitive, requires networks of neurons to generate new activity patterns. As some behaviours are easier to learn than others, we asked if some neural activity patterns are easier to generate than others. Here we investigate whether an existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define this constraint. We employed a closed-loop intracortical brain-computer interface learning paradigm in which Rhesus macaques (Macaca mulatta) controlled a computer cursor by modulating neural activity patterns in the primary motor cortex. Using the brain-computer interface paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. The activity of a neural population can be represented in a high-dimensional space (termed the neural space), wherein each dimension corresponds to the activity of one neuron. These characteristic activity patterns comprise a low-dimensional subspace (termed the intrinsic manifold) within the neural space. The intrinsic manifold presumably reflects constraints imposed by the underlying neural circuitry. Here we show that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the intrinsic manifold. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the intrinsic manifold. These results suggest that the existing structure of a network can shape learning. On a timescale of hours, it seems to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess.
authors.affiliation: 1] Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA [2] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [3] Systems Neuroscience Institute, University of Pittsburgh, Pittsburgh Pennsylvania 15261, USA.
authors.forename: Patrick T
authors.initials: PT
authors.lastname: Sadtler
authors.affiliation: 1] Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA [2] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [3] Systems Neuroscience Institute, University of Pittsburgh, Pittsburgh Pennsylvania 15261, USA.
authors.forename: Kristin M
authors.initials: KM
authors.lastname: Quick
authors.affiliation: 1] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [2] Department of Electrical and Computer Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Matthew D
authors.initials: MD
authors.lastname: Golub
authors.affiliation: 1] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [2] Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Steven M
authors.initials: SM
authors.lastname: Chase
authors.affiliation: 1] Department of Electrical Engineering, Stanford University, Stanford, California 94305, USA [2] Department of Neurosurgery, Palo Alto Medical Foundation, Palo Alto, California 94301, USA.
authors.forename: Stephen I
authors.initials: SI
authors.lastname: Ryu
authors.affiliation: 1] Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA [2] Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania 15213, USA [3] Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Elizabeth C
authors.initials: EC
authors.lastname: Tyler-Kabara
authors.affiliation: 1] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [2] Department of Electrical and Computer Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA [3] Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA [4].
authors.forename: Byron M
authors.initials: BM
authors.lastname: Yu
authors.affiliation: 1] Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA [2] Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, USA [3] Systems Neuroscience Institute, University of Pittsburgh, Pittsburgh Pennsylvania 15261, USA [4].
authors.forename: Aaron P
authors.initials: AP
authors.lastname: Batista
mesh_terms: D000818:Animals; D062207:Brain-Computer Interfaces; D003201:Computers; D007858:Learning / Q000502:physiology*; D008253:Macaca mulatta; D008297:Male; D008959:Models, Neurological; D009044:Motor Cortex / Q000166:cytology / Q000502:physiology; D009048:Motor Skills / Q000502:physiology*; D009415:Nerve Net / Q000166:cytology / Q000502:physiology; D009474:Neurons / Q000502:physiology