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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FULL STORY ==========================================================================
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.

* RELATED_TOPICS
o Mind_&_Brain
# Brain-Computer_Interfaces # Intelligence # Brain_Injury
# Memory # Neuroscience # Disorders_and_Syndromes #
Psychology # Dementia
* RELATED_TERMS
o Neural_network o Artificial_neural_network o
Computational_neuroscience o Memory_bias o Neuron o
Multiple_sclerosis o Sensory_system o Neurobiology

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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 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2023/07/230710113303.htm

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