TY - JOUR
T1 - Categorical signaling of the strongest stimulus by an inhibitory midbrain nucleus
AU - Schryver, Hannah M.
AU - Straka, Malgorzata
AU - Mysore, Shreesh P.
N1 - Funding Information:
Received Jan. 5, 2020; revised Mar. 4, 2020; accepted Apr. 2, 2020. Author contributions: S.P.M., H.M.S., and M.S. designed research; H.M.S. and M.S. performed research; H.M.S. and S.P.M. contributed unpublished reagents/analytic tools; H.M.S. and S.P.M. analyzed data; S.P.M. and H.M.S. wrote the paper. The authors declare no competing financial interests. This work was supported by funding from National Institutes of Health Grant R01-EY-027718. We thank James Garmon for assistance in building the equipment necessary for the experiments and Nagaraj Mahajan for help in data collection and analysis. M. Straka’s present address: Paradromics, Inc., Austin, TX 78759. Correspondence should be addressed to Shreesh P. Mysore at shreesh.mysore@jhu.edu. https://doi.org/10.1523/JNEUROSCI.0042-20.2020 Copyright © 2020 the authors
Publisher Copyright:
Copyright © 2020 the authors
PY - 2020/5/20
Y1 - 2020/5/20
N2 - The nucleus isthmi pars magnocellularis (Imc), a group of inhibitory neurons in the midbrain tegmentum, is a critical component of the spatial selection network in the vertebrate midbrain. It delivers long-range inhibition among different portions of the space map in the optic tectum (OT), thereby mediating stimulus competition in the OT. Here, we investigate the properties of relative strength-dependent competitive interactions within the Imc, in barn owls of both sexes. We find that when Imc neurons are presented simultaneously with one stimulus inside the receptive field and a second, competing stimulus outside, they exhibit gradual or switch-like response profiles as a function of relative stimulus strength. They do so both when the two stimuli are of the same sensory modality (both visual) or of different sensory modalities (visual and auditory). Moreover, Imc neurons signal the strongest stimulus in a dynamically flexible manner, indicating that Imc responses reflect an online comparison between the strengths of the competing stimuli. Notably, Imc neurons signal the strongest stimulus more categorically, and earlier than the OT. Paired recordings at spatially aligned sites in the Imc and OT reveal that although some properties of stimulus competition, such as the bias of competitive response profiles, are correlated, others such as the steepness of response profiles, are set independently. Our results demonstrate that the Imc is itself an active site of competition, and may be the first site in the midbrain selection network at which stimulus competition is resolved.
AB - The nucleus isthmi pars magnocellularis (Imc), a group of inhibitory neurons in the midbrain tegmentum, is a critical component of the spatial selection network in the vertebrate midbrain. It delivers long-range inhibition among different portions of the space map in the optic tectum (OT), thereby mediating stimulus competition in the OT. Here, we investigate the properties of relative strength-dependent competitive interactions within the Imc, in barn owls of both sexes. We find that when Imc neurons are presented simultaneously with one stimulus inside the receptive field and a second, competing stimulus outside, they exhibit gradual or switch-like response profiles as a function of relative stimulus strength. They do so both when the two stimuli are of the same sensory modality (both visual) or of different sensory modalities (visual and auditory). Moreover, Imc neurons signal the strongest stimulus in a dynamically flexible manner, indicating that Imc responses reflect an online comparison between the strengths of the competing stimuli. Notably, Imc neurons signal the strongest stimulus more categorically, and earlier than the OT. Paired recordings at spatially aligned sites in the Imc and OT reveal that although some properties of stimulus competition, such as the bias of competitive response profiles, are correlated, others such as the steepness of response profiles, are set independently. Our results demonstrate that the Imc is itself an active site of competition, and may be the first site in the midbrain selection network at which stimulus competition is resolved.
KW - Categorization
KW - Inhibition
KW - Midbrain
KW - Selection
KW - Spatial attention
KW - Superior colliculus
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U2 - 10.1523/JNEUROSCI.0042-20.2020
DO - 10.1523/JNEUROSCI.0042-20.2020
M3 - Article
C2 - 32300047
AN - SCOPUS:85085263860
SN - 0270-6474
VL - 40
SP - 4172
EP - 4184
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 21
ER -