MSGID: 1:317/3 64acdb27   
   PID: hpt/lnx 1.9.0-cur 2019-01-08   
   TID: hpt/lnx 1.9.0-cur 2019-01-08   
    Brain networks encoding memory come together via electric fields    
      
     Date:   
         July 10, 2023   
     Source:   
         Picower Institute at MIT   
     Summary:   
         New research provides evidence that electric fields shared among   
         neurons via 'ephaptic coupling' provide the coordination necessary   
         to assemble the multi-region neural ensembles ('engrams') that   
         represent remembered information.   
      
      
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   The "circuit" metaphor of the brain is as indisputable as it is familiar:   
   Neurons forge direct physical connections to create functional networks,   
   for instance to store memories or produce thoughts. But the metaphor   
   is also incomplete. What drives these circuits and networks to come   
   together? New evidence suggests that at least some of this coordination   
   comes from electric fields.   
      
   The new study in Cerebral Cortex shows that as animals played working   
   memory games, the information about what they were remembering was   
   coordinated across two key brain regions by the electric field that   
   emerged from the underlying electrical activity of all participating   
   neurons. The field, in turn, appeared to drive the neural activity,   
   or the fluctuations of voltage apparent across the cells' membranes.   
      
   If the neurons are musicians in an orchestra, the brain regions are   
   their sections, and the memory is the music they produce, the study's   
   authors said, then the electric field is the conductor.   
      
   The physical mechanism by which this prevailing electric field   
   influences the membrane voltage of constituent neurons is called   
   "ephaptic coupling." Those membrane voltages are fundamental to brain   
   activity. When they cross a threshold, neurons "spike," sending an   
   electrical transmission that signals other neurons across connections   
   called synapses. But any amount of electrical activity could contribute   
   to a prevailing electric field which also influences the spiking, said   
   study senior author Earl K. Miller, Picower Professor in the Department   
   of Brain and Cognitive Sciences at MIT.   
      
   "Many cortical neurons spend a lot of time wavering on verge of spiking"   
   Miller said. "Changes in their surrounding electric field can push them   
   one way or another. It's hard to imagine evolution not exploiting that."   
   In particular, the new study showed that the electric fields drove   
   the electrical activity of networks of neurons to produce a shared   
   representation of the information stored in working memory, said lead   
   author Dimitris Pinotsis, Associate Professor at City -- University   
   of London and a research affiliate in the Picower Institute. He noted   
   that the findings could improve the ability of scientists and engineers   
   to read information from the brain, which could help in the design of   
   brain-controlled prosthetics for people with paralysis.   
      
   "Using the theory of complex systems and mathematical pen and paper   
   calculations, we predicted that the brain's electric fields guide   
   neurons to produce memories," Pinotsis said. "Our experimental data   
   and statistical analyses support this prediction. This is an example   
   of how mathematics and physics shed light on the brain's fields and   
   how they can yield insights for building brain-computer interface   
   (BCI) devices."  Fields prevail In a 2022 study, Miller and Pinotsis   
   developed a biophysical model of the electric fields produced by neural   
   electrical activity. They showed that the overall fields that emerged   
   from groups of neurons in a brain region were more reliable and stable   
   representations of the information animals used to play working memory   
   games than the electrical activity of the individual neurons.   
      
   Neurons are somewhat fickle devices whose vagaries produce an information   
   inconsistency called "representational drift." In an opinion article   
   earlier this year, the scientists also posited that in addition to   
   neurons, electric fields affected the brain's molecular infrastructure   
   and its tuning so that the brain processes information efficiently.   
      
   In the new study, Pinotsis and Miller extended their inquiry to asking   
   whether ephaptic coupling spreads the governing electric field across   
   multiple brain regions to form a memory network, or "engram."  They   
   therefore broadened their analyses to look at two regions in the brain:   
   The frontal eye fields (FEF) and the supplementary eye fields (SEF). These   
   two regions, which govern voluntary movement of the eyes, were relevant to   
   the working memory game the animals were playing because in each round   
   the animals would see an image on a screen positioned at some angle   
   around the center (like the numbers on a clock). After a brief delay,   
   they had to glance in the same direction that the object had just been in.   
      
   As the animals played, the scientists recorded the local field potentials   
   (LFPs, a measure of local electrical activity) produced by scores of   
   neurons in each region. The scientists fed this recorded LFP data into   
   mathematical models that predicted individual neural activity and the   
   overall electric fields.   
      
   The models allowed Pinotsis and Miller to then calculate whether   
   changes in the fields predicted changes in the membrane voltages, or   
   whether changes in that activity predicted changes in the fields. To   
   do this analysis, they used a mathematical method called Granger   
   Causality. Unambiguously this analysis showed that in each region, the   
   fields had strong causal influence over the neural activity and not the   
   other way around. Consistent with last year's study, the analysis also   
   showed that measures of the strength of influence remained much steadier   
   for the fields than for the neural activity, indicating that fields were   
   more reliable.   
      
   The researchers then checked causality between the two brain regions and   
   found that electric fields, but not neural activity, reliably represented   
   the transfer of information between FEF and SEF. More specifically,   
   they found that the transfer typically flowed from FEF to SEF, which   
   agrees with prior studies of how the two regions interact. FEF tends to   
   lead the way in initiating an eye movement.   
      
   Finally, Pinotsis and Miller used another mathematical technique   
   called representation similarity analysis to determine whether the   
   two regions were, in fact, processing the same memory. They found that   
   the electric fields, but not the LFPs or neural activity, represented   
   the same information across both regions, unifying them into an engram   
   memory network.   
      
   Further clinical implications Considering evidence that electric fields   
   emerge from neural electrical activity but then come to drive neural   
   activity to represent information, Miller speculated that perhaps a   
   function of electrical activity in individual neurons is to produce the   
   fields that then govern them.   
      
   "It's a two-way street," Miller said. "The spiking and synapses are   
   very important. That's the foundation. But then the fields turn around   
   and influence the spiking."  That could have important implications for   
   mental health treatments, he said, because whether and when neurons spike,   
   influences the strength of their connections and thereby the function   
   of the circuits they form, a phenomenon called synaptic plasticity.   
      
   Clinical technologies such as transcranial electrical stimulation   
   (TES) alter brain electrical fields, Miller noted. If electrical   
   fields not only reflect neural activity but actively shape it, then   
   TES technologies could be used to alter circuits. Properly devised   
   electrical field manipulations, he said, could one day help patients   
   rewire faulty circuits.   
      
   Funding for the study came from UK Research and Innovation, the   
   U.S. Office of Naval Research, The JPB Foundation and The Picower   
   Institute for Learning and Memory.   
      
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   Journal Reference:   
      1. Dimitris A Pinotsis, Earl K Miller. In vivo ephaptic coupling allows   
         memory network formation. Cerebral Cortex, 2023; DOI:   
         10.1093/cercor/ bhad251   
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   Link to news story:   
   https://www.sciencedaily.com/releases/2023/07/230710113303.htm   
      
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