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The headache and sensory amplifications of migraine are attributed to hyperexcitable sensory circuits, but a detailed understanding remains elusive. A mutation in casein kinase 1 delta (CK1\u03b4) was identified in non-hemiplegic familial migraine with aura and advanced sleep phase syndrome. Mice carrying the CK1\u03b4T44A mutation were more susceptible to spreading depolarization (the phenomenon that underlies migraine aura), but mechanisms underlying this migraine-relevant phenotype were not known. We used a combination of whole-cell electrophysiology and multiphoton imaging, in vivo and in brain slices, to compare CK1\u03b4T44A mice (adult males) to their wild-type littermates.<\/jats:p>\n                  <jats:p>We found that despite comparable synaptic activity at rest, CK1\u03b4T44A neurons were more excitable upon repetitive stimulation than wild-type, with a reduction in presynaptic adaptation at excitatory but not inhibitory synapses. The mechanism of this adaptation deficit was a calcium-dependent enhancement of the size of the readily releasable pool of synaptic vesicles, and a resultant increase in glutamate release, in CK1\u03b4T44A compared to wild-type synapses. Consistent with this mechanism, CK1\u03b4T44A neurons showed an increase in the cumulative amplitude of excitatory post-synaptic currents, and a higher excitation-to-inhibition ratio during sustained activity compared to wild-type.<\/jats:p>\n                  <jats:p>At a local circuit level, action potential bursts elicited in CK1\u03b4T44A neurons triggered an increase in recurrent excitation compared to wild-type, and at a network level, CK1\u03b4T44A mice showed a longer duration of \u2018up state\u2019 activity, which is dependent on recurrent excitation. Finally, we demonstrated that the spreading depolarization susceptibility of CK1\u03b4T44A mice could be returned to wild-type levels with the same intervention (reduced extracellular calcium) that normalized presynaptic adaptation.<\/jats:p>\n                  <jats:p>Taken together, these findings show a stimulus-dependent presynaptic gain of function at glutamatergic synapses in a genetic model of migraine, that accounts for the increased spreading depolarization susceptibility and may also explain the sensory amplifications that are associated with the disease.<\/jats:p>","DOI":"10.1093\/brain\/awad326","type":"journal-article","created":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T20:43:18Z","timestamp":1697056998000},"page":"680-697","source":"Crossref","is-referenced-by-count":12,"title":["Increased presynaptic excitability in a migraine with aura mutation"],"prefix":"10.1093","volume":"147","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6904-7294","authenticated-orcid":false,"given":"Pratyush","family":"Suryavanshi","sequence":"first","affiliation":[{"name":"Department of Neurology, University of Utah School of Medicine , Salt Lake City, UT 84132 , USA"},{"name":"Interdepartmental Neuroscience Program, University of Utah School of Medicine , Salt Lake City, UT 84132 , USA"},{"name":"Department of Pediatrics, University of Iowa , Iowa City, IA 52242 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Punam","family":"Sawant-Pokam","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Utah School of Medicine , Salt Lake City, UT 84132 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Clair","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Utah School of Medicine , Salt Lake City, UT 84132 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4193-5841","authenticated-orcid":false,"given":"K C","family":"Brennan","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Utah School of Medicine , Salt Lake City, UT 84132 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,10,13]]},"reference":[{"key":"2024020201481908600_awad326-B1","doi-asserted-by":"crossref","first-page":"2443","DOI":"10.1001\/jama.290.18.2443","article-title":"Lost productive time and cost due to common pain conditions in the US workforce","volume":"290","author":"Stewart","year":"2003","journal-title":"JAMA"},{"key":"2024020201481908600_awad326-B2","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1212\/01.wnl.0000252808.97649.21","article-title":"Migraine prevalence, disease burden, and the need for preventive 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