Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat.
Substantia gelatinosa (SG, lamina II) is a spinal cord region where most unmyelinated primary afferents terminate and the central nociceptive processing begins. It is formed by several distinct groups of interneurons whose functional properties and synaptic connections are poorly understood, in part, because recordings from synaptically coupled pairs of SG neurons are quite challenging due to a very low probability of finding connected cells. Here, we describe an efficient method for identifying synaptically coupled interneurons in rat spinal cord slices and characterizing their excitatory or inhibitory function. Using tight-seal whole-cell recordings and a cell-attached stimulation technique, we routinely tested about 1500 SG interneurons, classifying 102 of them as monosynaptically connected to neurons in lamina I-III. Surprisingly, the vast majority of SG interneurons (n = 87) were excitatory and glutamatergic, while only 15 neurons were inhibitory. According to their intrinsic firing properties, these 102 SG neurons were also classified as tonic (n = 49), adapting (n = 17) or delayed-firing neurons (n = 36). All but two tonic neurons and all adapting neurons were excitatory interneurons. Of 36 delayed-firing neurons, 23 were excitatory and 13 were inhibitory. We conclude that sensory integration in the intrinsic SG neuronal network is dominated by excitatory interneurons. Such organization of neuronal circuitries in the spinal SG can be important for nociceptive encoding.
Santos
Sónia F A
SF
Instituto de Biologia Molecular e Celular-IBMC, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal.
Rebelo
Sandra
S
Derkach
Victor A
VA
Safronov
Boris V
BV
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000818:Animals; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D018756:GABA Antagonists / Q000494:pharmacology; D005971:Glutamates / Q000502:physiology*; D018684:Glycine Agents / Q000494:pharmacology; D007395:Interneurons / Q000166:cytology / Q000502:physiology*; D009475:Neurons, Afferent / Q000166:cytology / Q000502:physiology*; D018408:Patch-Clamp Techniques; D010852:Picrotoxin / Q000494:pharmacology; D017729:Presynaptic Terminals / Q000187:drug effects / Q000502:physiology; D051381:Rats; D013331:Strychnine / Q000494:pharmacology; D013376:Substantia Gelatinosa / Q000166:cytology / Q000502:physiology*
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D005971:Glutamates; D018684:Glycine Agents; D010852:Picrotoxin; D013331:Strychnine