Action of brain stem reticular afferents on lagged and nonlagged cells in the cat lateral geniculate nucleus

A. L. Humphrey, Alan B Saul

Research output: Contribution to journalArticle

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Abstract

1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (X(L)) and nonlagged X- and Y-cells (X(N) and Y(N)). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was >50% in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for X(N)-cells than for Y(N)- and X(L)-cells, reflecting the relatively higher discharge rate among X(N)-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among X(N)- and Y(N)-cells, PB stimulation had no significant effect on these two latencies; among X(L)-cells, both latencies were reduced by 43 and 35%, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies >60 ms. Despite the reduction among X(L)-cells in these 2 latencies during PB stimulation, all but 2 of the 40 X(L)-cells maintained laggedlike latencies. The majority (95%) of X(L)-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 X(L)-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting ~45 ms after spot onset. During PB stimulation only three cells lost the dip. In the remaining cells, dip duration and amplitude were markedly reduced, by 57 and 23%, respectively, but the onset latency of the dip was unchanged. We interpret this as suggesting that the inhibitory mechanisms that initiate the dip are largely exempt from brain stem influence, whereas the mechanisms that sustain the dip are more susceptible to brain stem action. 6. As a control, we measured the amplitude and timing of PB-evoked facilitation in the absence of visual stimulation. Lagged and nonlagged cells were similar in responding with a four-fold increase in mean discharge rate; this increase often outlasted the PB stimulus train by many (3-12) seconds. The long duration of facilitation is consistent with a cholinergic muscarinic action mediated by afferents from PB. For most cells the onset of facilitation occurred within 60 ms of PB onset. Because we initiated PB stimulation 100 ms before spot onset, we are confident that the brain stem action was appropriately timed to facilitate spot-evoked responses. That is, the fact that nearly all X(L)-cells remained lagged during PB stimulation was not due to inappropriate timing of the brain stem and visual stimuli. 7. We conclude that brain stem-geniculate afferents have a strong facilitatory action on lagged and nonlagged cells. They reduce inhibition on lagged cells and shorten the cells' discharge latencies, drawing them closer to nonlagged cells in response amplitude and timing. However, with very few exceptions, the lagged and nonlagged cells remain readily distinguishable as separate groups during brain stem activation.

Original languageEnglish (US)
Pages (from-to)673-691
Number of pages19
JournalJournal of Neurophysiology
Volume68
Issue number3
DOIs
StatePublished - Jan 1 1992
Externally publishedYes

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Geniculate Bodies
Brain Stem
Cats

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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Action of brain stem reticular afferents on lagged and nonlagged cells in the cat lateral geniculate nucleus. / Humphrey, A. L.; Saul, Alan B.

In: Journal of Neurophysiology, Vol. 68, No. 3, 01.01.1992, p. 673-691.

Research output: Contribution to journalArticle

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title = "Action of brain stem reticular afferents on lagged and nonlagged cells in the cat lateral geniculate nucleus",
abstract = "1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (X(L)) and nonlagged X- and Y-cells (X(N) and Y(N)). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was >50{\%} in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for X(N)-cells than for Y(N)- and X(L)-cells, reflecting the relatively higher discharge rate among X(N)-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among X(N)- and Y(N)-cells, PB stimulation had no significant effect on these two latencies; among X(L)-cells, both latencies were reduced by 43 and 35{\%}, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies >60 ms. Despite the reduction among X(L)-cells in these 2 latencies during PB stimulation, all but 2 of the 40 X(L)-cells maintained laggedlike latencies. The majority (95{\%}) of X(L)-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 X(L)-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting ~45 ms after spot onset. During PB stimulation only three cells lost the dip. In the remaining cells, dip duration and amplitude were markedly reduced, by 57 and 23{\%}, respectively, but the onset latency of the dip was unchanged. We interpret this as suggesting that the inhibitory mechanisms that initiate the dip are largely exempt from brain stem influence, whereas the mechanisms that sustain the dip are more susceptible to brain stem action. 6. As a control, we measured the amplitude and timing of PB-evoked facilitation in the absence of visual stimulation. Lagged and nonlagged cells were similar in responding with a four-fold increase in mean discharge rate; this increase often outlasted the PB stimulus train by many (3-12) seconds. The long duration of facilitation is consistent with a cholinergic muscarinic action mediated by afferents from PB. For most cells the onset of facilitation occurred within 60 ms of PB onset. Because we initiated PB stimulation 100 ms before spot onset, we are confident that the brain stem action was appropriately timed to facilitate spot-evoked responses. That is, the fact that nearly all X(L)-cells remained lagged during PB stimulation was not due to inappropriate timing of the brain stem and visual stimuli. 7. We conclude that brain stem-geniculate afferents have a strong facilitatory action on lagged and nonlagged cells. They reduce inhibition on lagged cells and shorten the cells' discharge latencies, drawing them closer to nonlagged cells in response amplitude and timing. However, with very few exceptions, the lagged and nonlagged cells remain readily distinguishable as separate groups during brain stem activation.",
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N2 - 1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (X(L)) and nonlagged X- and Y-cells (X(N) and Y(N)). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was >50% in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for X(N)-cells than for Y(N)- and X(L)-cells, reflecting the relatively higher discharge rate among X(N)-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among X(N)- and Y(N)-cells, PB stimulation had no significant effect on these two latencies; among X(L)-cells, both latencies were reduced by 43 and 35%, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies >60 ms. Despite the reduction among X(L)-cells in these 2 latencies during PB stimulation, all but 2 of the 40 X(L)-cells maintained laggedlike latencies. The majority (95%) of X(L)-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 X(L)-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting ~45 ms after spot onset. During PB stimulation only three cells lost the dip. In the remaining cells, dip duration and amplitude were markedly reduced, by 57 and 23%, respectively, but the onset latency of the dip was unchanged. We interpret this as suggesting that the inhibitory mechanisms that initiate the dip are largely exempt from brain stem influence, whereas the mechanisms that sustain the dip are more susceptible to brain stem action. 6. As a control, we measured the amplitude and timing of PB-evoked facilitation in the absence of visual stimulation. Lagged and nonlagged cells were similar in responding with a four-fold increase in mean discharge rate; this increase often outlasted the PB stimulus train by many (3-12) seconds. The long duration of facilitation is consistent with a cholinergic muscarinic action mediated by afferents from PB. For most cells the onset of facilitation occurred within 60 ms of PB onset. Because we initiated PB stimulation 100 ms before spot onset, we are confident that the brain stem action was appropriately timed to facilitate spot-evoked responses. That is, the fact that nearly all X(L)-cells remained lagged during PB stimulation was not due to inappropriate timing of the brain stem and visual stimuli. 7. We conclude that brain stem-geniculate afferents have a strong facilitatory action on lagged and nonlagged cells. They reduce inhibition on lagged cells and shorten the cells' discharge latencies, drawing them closer to nonlagged cells in response amplitude and timing. However, with very few exceptions, the lagged and nonlagged cells remain readily distinguishable as separate groups during brain stem activation.

AB - 1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (X(L)) and nonlagged X- and Y-cells (X(N) and Y(N)). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was >50% in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for X(N)-cells than for Y(N)- and X(L)-cells, reflecting the relatively higher discharge rate among X(N)-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among X(N)- and Y(N)-cells, PB stimulation had no significant effect on these two latencies; among X(L)-cells, both latencies were reduced by 43 and 35%, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies >60 ms. Despite the reduction among X(L)-cells in these 2 latencies during PB stimulation, all but 2 of the 40 X(L)-cells maintained laggedlike latencies. The majority (95%) of X(L)-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 X(L)-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting ~45 ms after spot onset. During PB stimulation only three cells lost the dip. In the remaining cells, dip duration and amplitude were markedly reduced, by 57 and 23%, respectively, but the onset latency of the dip was unchanged. We interpret this as suggesting that the inhibitory mechanisms that initiate the dip are largely exempt from brain stem influence, whereas the mechanisms that sustain the dip are more susceptible to brain stem action. 6. As a control, we measured the amplitude and timing of PB-evoked facilitation in the absence of visual stimulation. Lagged and nonlagged cells were similar in responding with a four-fold increase in mean discharge rate; this increase often outlasted the PB stimulus train by many (3-12) seconds. The long duration of facilitation is consistent with a cholinergic muscarinic action mediated by afferents from PB. For most cells the onset of facilitation occurred within 60 ms of PB onset. Because we initiated PB stimulation 100 ms before spot onset, we are confident that the brain stem action was appropriately timed to facilitate spot-evoked responses. That is, the fact that nearly all X(L)-cells remained lagged during PB stimulation was not due to inappropriate timing of the brain stem and visual stimuli. 7. We conclude that brain stem-geniculate afferents have a strong facilitatory action on lagged and nonlagged cells. They reduce inhibition on lagged cells and shorten the cells' discharge latencies, drawing them closer to nonlagged cells in response amplitude and timing. However, with very few exceptions, the lagged and nonlagged cells remain readily distinguishable as separate groups during brain stem activation.

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