TY - JOUR
T1 - Synapse-type-specific competitive Hebbian learning forms functional recurrent networks
AU - Eckmann, Samuel
AU - Young, Edward James
AU - Gjorgjieva, Julijana
N1 - Publisher Copyright:
Copyright © 2024 the Author(s).
PY - 2024/6/1
Y1 - 2024/6/1
N2 - Cortical networks exhibit complex stimulus–response patterns that are based on specific recurrent interactions between neurons. For example, the balance between excitatory and inhibitory currents has been identified as a central component of cortical computations. However, it remains unclear how the required synaptic connectivity can emerge in developing circuits where synapses between excitatory and inhibitory neurons are simultaneously plastic. Using theory and modeling, we propose that a wide range of cortical response properties can arise from a single plasticity paradigm that acts simultaneously at all excitatory and inhibitory connections—Hebbian learning that is stabilized by the synapse-type-specific competition for a limited supply of synaptic resources. In plastic recurrent circuits, this competition enables the formation and decorrelation of inhibition-balanced receptive fields. Networks develop an assembly structure with stronger synaptic connections between similarly tuned excitatory and inhibitory neurons and exhibit response normalization and orientation-specific center-surround suppression, reflecting the stimulus statistics during training. These results demonstrate how neurons can self-organize into functional networks and suggest an essential role for synapse-type-specific competitive learning in the development of cortical circuits.
AB - Cortical networks exhibit complex stimulus–response patterns that are based on specific recurrent interactions between neurons. For example, the balance between excitatory and inhibitory currents has been identified as a central component of cortical computations. However, it remains unclear how the required synaptic connectivity can emerge in developing circuits where synapses between excitatory and inhibitory neurons are simultaneously plastic. Using theory and modeling, we propose that a wide range of cortical response properties can arise from a single plasticity paradigm that acts simultaneously at all excitatory and inhibitory connections—Hebbian learning that is stabilized by the synapse-type-specific competition for a limited supply of synaptic resources. In plastic recurrent circuits, this competition enables the formation and decorrelation of inhibition-balanced receptive fields. Networks develop an assembly structure with stronger synaptic connections between similarly tuned excitatory and inhibitory neurons and exhibit response normalization and orientation-specific center-surround suppression, reflecting the stimulus statistics during training. These results demonstrate how neurons can self-organize into functional networks and suggest an essential role for synapse-type-specific competitive learning in the development of cortical circuits.
KW - excitation–inhibition balance
KW - recurrent networks
KW - surround suppression
KW - synaptic plasticity
UR - http://www.scopus.com/inward/record.url?scp=85196137802&partnerID=8YFLogxK
U2 - 10.1073/pnas.2305326121
DO - 10.1073/pnas.2305326121
M3 - Article
C2 - 38870059
AN - SCOPUS:85196137802
SN - 0027-8424
VL - 121
SP - 1
EP - 12
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 25
M1 - e2305326121
ER -