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A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement.

Butts DA, Kanold PO, Shatz CJ - PLoS Biol. (2007)

Bottom Line: Using perforated patch recordings from neurons in LGN slices during the period of eye segregation, we examine how such burst-based activity can instruct this refinement.It is consistent with "Hebbian" development thought to exist at this synapse, and we demonstrate computationally that such a rule can robustly use retinal waves to drive eye segregation and retinotopic refinement.Thus, by measuring plasticity induced by natural activity patterns, synaptic learning rules can be linked directly to their larger role in instructing the patterning of neural connectivity.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America. dab2024@med.cornell.edu

ABSTRACT
Patterned spontaneous activity in the developing retina is necessary to drive synaptic refinement in the lateral geniculate nucleus (LGN). Using perforated patch recordings from neurons in LGN slices during the period of eye segregation, we examine how such burst-based activity can instruct this refinement. Retinogeniculate synapses have a novel learning rule that depends on the latencies between pre- and postsynaptic bursts on the order of one second: coincident bursts produce long-lasting synaptic enhancement, whereas non-overlapping bursts produce mild synaptic weakening. It is consistent with "Hebbian" development thought to exist at this synapse, and we demonstrate computationally that such a rule can robustly use retinal waves to drive eye segregation and retinotopic refinement. Thus, by measuring plasticity induced by natural activity patterns, synaptic learning rules can be linked directly to their larger role in instructing the patterning of neural connectivity.

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Generating In Vivo Activity Patterns(A) Schematic demonstrating natural activity resulting from retinal waves in the retina (top) and LGN (bottom): a retinal wave involves activity over a population of RGCs (#1) that evokes a large synaptic input in target LGN neurons (#2). Dashed boxes correspond to the two components of natural retinal wave activity reproduced in our experiments. Retinal wave multi-electrode recording data were adapted from Wong et al. [14]; LGN synaptic recording adapted from Mooney et al. [30](B) Retinal wave activity at the retinogeniculate synapse is reproduced by minimal 10-Hz stimulation to the OT (vertical blue lines) paired at a given latency with direct current injection into the recorded LGN neuron to evoke 10–20 Hz bursting (top). Participation of the selected synapse has negligible effect on LGN firing, as shown by comparing the depolarization paired with +100 ms latency OT stimulation (stim) (top) with depolarization alone (bottom).(C) This situation is in marked contrast to a tetanus protocol, which involves higher current stimulation (100 Hz for 1 s), resulting in a long-lasting depolarization largely absent of postsynaptic spiking.Scale bars for (B) and (C) are shown between these panels.
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pbio-0050061-g001: Generating In Vivo Activity Patterns(A) Schematic demonstrating natural activity resulting from retinal waves in the retina (top) and LGN (bottom): a retinal wave involves activity over a population of RGCs (#1) that evokes a large synaptic input in target LGN neurons (#2). Dashed boxes correspond to the two components of natural retinal wave activity reproduced in our experiments. Retinal wave multi-electrode recording data were adapted from Wong et al. [14]; LGN synaptic recording adapted from Mooney et al. [30](B) Retinal wave activity at the retinogeniculate synapse is reproduced by minimal 10-Hz stimulation to the OT (vertical blue lines) paired at a given latency with direct current injection into the recorded LGN neuron to evoke 10–20 Hz bursting (top). Participation of the selected synapse has negligible effect on LGN firing, as shown by comparing the depolarization paired with +100 ms latency OT stimulation (stim) (top) with depolarization alone (bottom).(C) This situation is in marked contrast to a tetanus protocol, which involves higher current stimulation (100 Hz for 1 s), resulting in a long-lasting depolarization largely absent of postsynaptic spiking.Scale bars for (B) and (C) are shown between these panels.

Mentions: Using perforated patch recording from an in vitro slice preparation of the LGN and optic tract (OT), the effects of the natural activity patterns produced by retinal waves on selected retinogeniculate synapses were examined. Throughout most of the period of eye segregation, RGCs provide the major source of driven input to the LGN [28,29]; as a result, the population-level imaging of retinal waves provides a full view of the spatiotemporal dynamics across the inputs to LGN neurons (Figure 1A). In LGN neurons, these inputs manifest as large synaptic currents lasting seconds, and evoke bursts of action potentials in response [30]. Thus, to replicate the effects of retinal waves on the synapse, we combined minimal stimulation of the OT (to activate one or a few synapses) with direct current injection into the LGN neuron (to simulate the remainder of the inputs). Such current injection was adjusted to evoke physiologically appropriate LGN activity: 10–20 Hz spiking for 1 s [30].


A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement.

Butts DA, Kanold PO, Shatz CJ - PLoS Biol. (2007)

Generating In Vivo Activity Patterns(A) Schematic demonstrating natural activity resulting from retinal waves in the retina (top) and LGN (bottom): a retinal wave involves activity over a population of RGCs (#1) that evokes a large synaptic input in target LGN neurons (#2). Dashed boxes correspond to the two components of natural retinal wave activity reproduced in our experiments. Retinal wave multi-electrode recording data were adapted from Wong et al. [14]; LGN synaptic recording adapted from Mooney et al. [30](B) Retinal wave activity at the retinogeniculate synapse is reproduced by minimal 10-Hz stimulation to the OT (vertical blue lines) paired at a given latency with direct current injection into the recorded LGN neuron to evoke 10–20 Hz bursting (top). Participation of the selected synapse has negligible effect on LGN firing, as shown by comparing the depolarization paired with +100 ms latency OT stimulation (stim) (top) with depolarization alone (bottom).(C) This situation is in marked contrast to a tetanus protocol, which involves higher current stimulation (100 Hz for 1 s), resulting in a long-lasting depolarization largely absent of postsynaptic spiking.Scale bars for (B) and (C) are shown between these panels.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808114&req=5

pbio-0050061-g001: Generating In Vivo Activity Patterns(A) Schematic demonstrating natural activity resulting from retinal waves in the retina (top) and LGN (bottom): a retinal wave involves activity over a population of RGCs (#1) that evokes a large synaptic input in target LGN neurons (#2). Dashed boxes correspond to the two components of natural retinal wave activity reproduced in our experiments. Retinal wave multi-electrode recording data were adapted from Wong et al. [14]; LGN synaptic recording adapted from Mooney et al. [30](B) Retinal wave activity at the retinogeniculate synapse is reproduced by minimal 10-Hz stimulation to the OT (vertical blue lines) paired at a given latency with direct current injection into the recorded LGN neuron to evoke 10–20 Hz bursting (top). Participation of the selected synapse has negligible effect on LGN firing, as shown by comparing the depolarization paired with +100 ms latency OT stimulation (stim) (top) with depolarization alone (bottom).(C) This situation is in marked contrast to a tetanus protocol, which involves higher current stimulation (100 Hz for 1 s), resulting in a long-lasting depolarization largely absent of postsynaptic spiking.Scale bars for (B) and (C) are shown between these panels.
Mentions: Using perforated patch recording from an in vitro slice preparation of the LGN and optic tract (OT), the effects of the natural activity patterns produced by retinal waves on selected retinogeniculate synapses were examined. Throughout most of the period of eye segregation, RGCs provide the major source of driven input to the LGN [28,29]; as a result, the population-level imaging of retinal waves provides a full view of the spatiotemporal dynamics across the inputs to LGN neurons (Figure 1A). In LGN neurons, these inputs manifest as large synaptic currents lasting seconds, and evoke bursts of action potentials in response [30]. Thus, to replicate the effects of retinal waves on the synapse, we combined minimal stimulation of the OT (to activate one or a few synapses) with direct current injection into the LGN neuron (to simulate the remainder of the inputs). Such current injection was adjusted to evoke physiologically appropriate LGN activity: 10–20 Hz spiking for 1 s [30].

Bottom Line: Using perforated patch recordings from neurons in LGN slices during the period of eye segregation, we examine how such burst-based activity can instruct this refinement.It is consistent with "Hebbian" development thought to exist at this synapse, and we demonstrate computationally that such a rule can robustly use retinal waves to drive eye segregation and retinotopic refinement.Thus, by measuring plasticity induced by natural activity patterns, synaptic learning rules can be linked directly to their larger role in instructing the patterning of neural connectivity.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America. dab2024@med.cornell.edu

ABSTRACT
Patterned spontaneous activity in the developing retina is necessary to drive synaptic refinement in the lateral geniculate nucleus (LGN). Using perforated patch recordings from neurons in LGN slices during the period of eye segregation, we examine how such burst-based activity can instruct this refinement. Retinogeniculate synapses have a novel learning rule that depends on the latencies between pre- and postsynaptic bursts on the order of one second: coincident bursts produce long-lasting synaptic enhancement, whereas non-overlapping bursts produce mild synaptic weakening. It is consistent with "Hebbian" development thought to exist at this synapse, and we demonstrate computationally that such a rule can robustly use retinal waves to drive eye segregation and retinotopic refinement. Thus, by measuring plasticity induced by natural activity patterns, synaptic learning rules can be linked directly to their larger role in instructing the patterning of neural connectivity.

Show MeSH
Related in: MedlinePlus