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bas ZiburkusDepartment of Cell Biology and Anatomy Louisiana State Health Sciences Center, New Orleans, Louisiana 70112
Submitted 25 February 2003; accepted in final form 17 April 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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). However, compared with our knowledge about the development
of excitatory activity in LGN, there is limited information about the ontogeny
of inhibitory activity during the period of retinogeniculate axon segregation.
In some mammalian species (e.g., ferret and cat), inhibitory activity seems to
initially appear during the late phases of retinogeniculate axon segregation
(Pirchio et al. 1997;
Ramoa and McCormick 1994;
Shatz and Kirkwood 1984; but
see White and Sur 1992) and
becomes more prevalent thereafter as LGN cells take on adult-like
receptive-field properties (Tavazoie and
Reid 2000; Tootle and
Friedlander 1986). In the cat, the emergence of inhibitory
activity at or near birth also corresponds to the appearance of glutamic acid
decarboxylase (GAD) staining in somata and terminals of A-layer LGN cells
(Shotwell et al. 1986). In the rat, the expression of GABAergic elements in
LGN occurs at earlier prenatal times
(Bentivoglio et al. 1991;
Lauder et al. 1986;
Laurie et al. 1992). This
suggests that in rodents inhibitory activity emerges earlier in development,
perhaps preceding or at least coinciding with the period of retinogeniculate
axon segregation (Guido et al.
2003; Guido and Ziburkus
2001; Jeffery
1984).
A number of other issues regarding the nature and origin of inhibitory
activity in the developing LGN remain unresolved. In the adult LGN, optic
tract stimulation evokes a monosynaptic excitatory postsynaptic potential
(EPSP) that is followed by two inhibitory postsynaptic potentials (IPSPs), an
early fast one mediated by a GABAA Cl– conductance
and a late slow one mediated by a GABAB K+ conductance
(Crunelli et al. 1988). It is
not clear whether these inhibitory events develop at different rates, or when
they do emerge, if they are part of a feed-forward circuit involving LGN
interneurons or a recurrent one involving neurons of the thalamic reticular
nucleus. Moreover, inhibitory activity in the LGN has been implicated in both
monocular and binocular signaling (e.g.,
Guido et al. 1989;
Xue et al. 1987). The
circuitry underlying binocular inhibitory interactions has received limited
attention (Lindström
1982). and its emergence during development has yet to be
investigated. To examine these issues, we studied the synaptic responses of
developing LGN cells in an in vitro isolated brain stem preparation
(Fig. 1)
(Lo et al. 2002; see also
Shatz and Kirkwood 1984 for a
similar preparation in the developing kitten). This preparation is especially
suited for the study of synaptic transmission because large segments of each
optic nerve as well as the intrinsic circuitry of the LGN remain intact.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Figure 1 depicts the isolated brain stem and our experimental approach. The excised brain was cut in half along the midline axis, glued to a silver plate, and placed into a well of a temperature-controlled recording chamber. The lateral surface of the thalamus and midbrain were exposed by removing the forebrain. The isolated brain stem was submerged and perfused continuously (4–5 ml/min) with warmed (31–33°C) ACSF. In experiments that required electrical stimulation of the optic nerves, the isolated brain stem preparation was modified to include large segments of each optic nerve (Fig. 1). The nerves were cut just behind the optic disk and dissected from the base of the skull, thus sparing at least 4–5 mm of each optic nerve. Using a ventral approach, the brain was cut along the midline axis while leaving the optic chiasm intact. Recordings began 1–3 h after incubation and were done at a depth of 50–250 µm below the pial surface of the LGN.
Whole cell recordings were obtained with pipettes made of borosillicate
glass filled with a solution containing (in mM) 140 K gluconate, 10 HEPES, 1.1
EGTA-Na, 0.1 CaCl2, 2 MgCl2, 2 ATP-Mg, 0.2 GTP-Na (pH =
7.2) and pulled to a final tip resistance 5–7 M
. In some cases,
we used sharp-tipped electrodes filled with either 4 M potassium acetate (KAC)
or a 2% solution of biocytin dissolved in 2 M KAC. Sharp-tipped electrodes
were pulled to a final tip resistance of 70–90 M. Intracellular
recordings were done in current clamp mode with an Axoclamp 2B amplifier using
techniques described elsewhere (Guido et al.
1997,
1998;
Lo et al. 2002). All neuronal
activity was displayed on a storage oscilloscope, digitized at 10 kHz, and
stored directly on computer.
During intracellular recording, some LGN cells (n = 18) were
filled with biocytin by passing alternating positive and negative current
pulses (±1nA, 30 ms, 100–300 pulses) through the recording
electrode. Tissue containing biocytin-filled cells was placed in a fixative
solution of 4% paraformaldehyde dissolved in 0.1 M phosphate buffer for 72 h.
The LGN was sectioned (400 µm) in the coronal plane and processed using the
ABC method (Guido et al. 1997;
Horikawa and Armstrong 1988).
Labeled cells were photographed and drawn using a camera lucida attached to a
microscope.
To evoke synaptic activity in LGN, single square-wave pulses (0.1–0.3
ms, 0.1-5.0 mA) were delivered at a rate of 0.20–1.0 Hz through a pair
of low-impedance (0.2–0.5 M), thin-gauged Ir wires the exposed
tips (0.1 mm) of which were placed on the surface of the optic tract or on
each optic nerve. For experiments involving the stimulation of optic nerves,
the electrodes were placed at least 3–5 mm from the chiasm, and the two
nerves were separated 
5 mm from each other. In evoking synaptic activity,
we first determined the minimum stimulus intensity needed to evoke a
postsynaptic response. We then adjusted current intensity in 1, 2, 5 or 10%
increments from this initial threshold value until an EPSP of maximal
amplitude was reached. Various ligand-gated antagonists were bath applied to
ascertain the pharmacology underlying EPSP
[N-methyl-D-aspartate (NMDA):
D(–)-2-amino-5-phosphonopentanoic acid (APV, 100 µM)] and
IPSP (GABAA: bicuculline, 10–25 µM, and GABAB:
2-hydroxysaclofen, 100 µM) activity.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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).
Representative voltages responses to intracellular current injection and a
synaptic response (at postnatal day 11) evoked by optic tract stimulation are
shown in Fig. 2. These
responses are typical of rodent relay cells
(Crunelli et al. 1987;
Williams et al. 1996). The
voltage responses to intracellular current injection reflect a number of
active membrane properties. These include low-threshold
Ca2+ spikes (Fig.
2A, T) and burst firing
(Fig. 2A, B), a mixed
cation conductance (Fig. 2A,
H) that prevents membrane hyperpolarization, and a transient
K+ conductance (Fig.
2A, A) that delays spike firing during membrane
hyperpolarization. Sustained membrane depolarization also evoked a train of
action potentials that showed frequency adaptation, due largely to the
activation of an after-hyperpolarizing (AHP,
Fig. 2A) response that
follows each action potential. Electrical stimulation of retinal afferents
also evoked postsynaptic responses typical of rodent relay cells
(Crunelli et al. 1988). After
postnatal day 11, the synaptic responses were comprised of EPSP/IPSP pairs
(Fig. 2B, see
following text for details). Figure 2,
C and D, provides some examples of LGN cells
filled with biocytin during intracellular recording. Labeled cells (n
= 18) had relatively large somata and multipolar dendritic arbors consistent
with those of class A thalamocortical cells
(Grossman et al. 1973;
Parnavelas et al. 1977;
Webster and Rowe 1984) In some
instances, we could also identify an axon exiting the LGN. Taken together,
these results indicate that our recordings were likely restricted to relay
cells.
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; Lo et al.
2002; Ramoa and McCormick
1994). Additional GABAB-mediated IPSPs emerged at
P3–4 but were not prevalent until after the first postnatal week
(Fig. 3, C and
D). GABAB-mediated IPSPs followed
GABAA IPSPs, were longer in duration (200–300 ms), reversed
at membrane levels more negative than –95 mV, and were blocked by the
application of hydroxysaclofen (n = 10). We used the preceding
measures as a means to distinguish different inhibitory responses
(Crunelli et al. 1988;
Lo et al. 2002;
Ramoa and McCormick 1994;
Zhu and Lo 1999). Figure 4 plots the incidence of GABAA- and GABAB-mediated inhibition as a function of age for 130 LGN cells. GABAA responses were present as early as P1–2 (31%) and showed a rapid increase thereafter so that by P5 nearly every cell (98%) expressed GABAA-mediated IPSPs. GABAB responses developed more slowly. At P1–2, these responses were rare (6%) but showed a gradual increase with age so by P9–10 all cells possessed GABAB activity.
We were also able to evoke synaptic responses by stimulating the optic
nerves in preparations where large segments of each optic nerve were preserved
(Fig. 1). This approach has
proven useful for determining whether developing LGN cells are binocularly
responsive. Developing LGN cells receive excitatory retinal input from both
eyes (Guido and Ziburkus 2001;
Guido et al. 2003). Moreover,
binocular excitatory responses are transient and show an age-related decrease
that coincides with the recession of uncrossed retinal projections
(ipsilateral eye) terminating in LGN (see
Table 1)
(Guido and Ziburkus 2001;
Guido et al. 2003). By P19,
LGN cells receive excitatory monocular input from the retina. Examples of the
binocular responses evoked by optic nerve (ON) stimulation at P11–P14
are shown in Figs. 5 and
6, A and B.
Separate stimulation of the contralateral or ipsilateral ON evoked an
EPSP/IPSP pair. In fact, between P11 and P14, a time when inhibitory responses
have fully matured, 58.9% of (79/134) LGN cells tested exhibited a binocularly
mediated EPSP/IPSP pair.
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It is important to note that binocular responses cannot be attributed to
inadvertent current spread. We preserved large segments of each ON
(Fig. 1) and could evoke
binocular responses at stimulus intensity levels that were at threshold for
evoking postsynaptic responses (0.1–0.5 mA). Moreover, when concurrent
shocks were delivered to each optic nerve (shocks are timed so that responses
are evoked at the same time), the excitatory component of the synaptic
response reflected a summation of the response evoked by each nerve separately
(n = 4). An example is shown in
Fig. 5. The amplitude of the
EPSP evoked by contralateral ON stimulation was 12 mV, to ipsilateral ON
stimulation was 8 mV, and to concurrent stimulation 19 was mV. If the
stimulating current was indeed spreading from one electrode across both optic
nerves, then stimulation of both nerves should lead to occlusion and a reduced
response (Shatz and Kirkwood
1984).
During the time when binocular excitatory responses were waning, we
encountered a subset of LGN cells in which contralateral ON stimulation evoked
an EPSP/IPSP pair and ipsilateral ON stimulation evoked only IPSP activity.
Although these responses were somewhat rare (5%, 12/244), they first appeared
at P12, and as shown in Table 1
became somewhat more prevalent during the third postnatal week of life (11.7%,
8/68). Examples of these binocularly mediated inhibitory responses are shown
in Fig. 6, C–F.
These binocularly mediated IPSPs were evoked at stimulus intensity levels that
were at threshold for evoking a postsynaptic response (0.1–0.5 mA) or at
levels that were 10 times greater than those used to evoke a threshold
response (Fig. 6, D and
E). The absence of an accompanying EPSP (preceding the
IPSP) at high levels of stimulation suggests some retinal afferents from the
ipsilateral eye synapse exclusively onto LGN interneurons
(Ahlsén et al. 1985;
Lindström 1982). In a
normal ACSF solution, IPSPs evoked by ipsilateral optic nerve stimulation had
both a short and long-lasting hyperpolarizing component
(Fig. 6, C and
D), suggesting that both GABAA and
GABAB receptors subtypes were involved (n = 3). Robust
IPSP activity was also evident during the bath application of bicuculline
(n = 9; Fig. 6, E and
F). These IPSPs were of long duration and reversed at
membrane levels more negative than –90 mV
(Fig. 6F), indicating
they were likely mediated by GABAB receptor activation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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It could be that the delayed onset of GABAB activity observed in
the present experiment is related to the response firing of interneurons
evoked by optic tract stimulation. There is some evidence to suggest that
GABAB-mediated postsynaptic responses favor repetitive burst-like
firing of presynaptic afferents (Bal et al.
1995; Huguenard and Prince
1994; Kim et al.
1997). Burst-induced GABAB responses in thalamic relay
cells involves a recurrent feedback circuit with interneurons of the thalamic
reticular nucleus. With regard to the present experiments, perhaps the absence
of GABAB activity at the earliest postnatal ages is related to an
inability of immature interneurons to fire burst discharges in response to
optic tract stimulation. Although such activity might be necessary to evoke
GABAB activity via the recurrent feedback circuit, it does not seem
required for the activation of GABAB responses evoked by a
feed-forward inhibitory pathway. Recordings from LGN interneurons indicate
that a single shock of optic tract evokes a unitary EPSP with a single spike
riding its peak (Lindström
1983; Williams et al.
1996; Zhu and Lo
1999), and this form of activation can reliably evoke robust
GABAB activity in relay cells
(Crunelli et al. 1987;
Lo et al. 2002;
Soltez et al. 1989). Moreover,
we have also shown that at early postnatal ages repetitive activation of the
optic tract is no more capable of evoking GABAB responses than
single shocks (Lo et al. 2002)
(Fig. 10). Typically, repetitive activation (20 and 50 Hz) of the optic tract
evokes a large plateau-like depolarization with no evidence of inhibition.
Finally, we have tested frequencies as high as 100 Hz and have seen no sign of
inhibition (n = 3, data not shown).
Although GABAA and GABAB inhibition develop at
different rates, overall the relatively early maturation of inhibitory
responses in the rat differs from that reported in other mammalian species.
For example, in the ferret, optic tract-evoked IPSP activity appears during
postnatal week 3–4 (Ramoa and
McCormick 1994; but see White
and Sur 1992), a time when retinogeniculate axon segregation is
nearly complete (Linden et al.
1981). A similar timing was found in the developing kitten. Using
an isolated diencephalon preparation and extracellular recording techniques,
Shatz and Kirkwood (1984) were
able to detect inhibitory activity near the late stage of gestation and early
postnatal life, a time when retinogeniculate axon segregation is adult-like
(Shatz 1983). By contrast, the
maturation of inhibitory responses in the rat seems to occur during the early
phases retinal axon segregation (Guido and
Ziburkus 2001; Guido et al.
2003; Jeffery
1984). Based on the anterograde labeling pattern of retinofugal
projections with the subunit B cholera toxin, we estimated that during the
first week of life the uncrossed retinal projections occupy between 50 and 90%
of LGN (Guido and Ziburkus
2001; Guido et al.
2003). The fact that inhibition in the LGN develops during early
(rat) and late phases (ferret and cat) of retinogeniculate axon segregation
suggests that such activity may not play a major role in the
activity-dependent consolidation of adult-like patterns of retinogeniculate
connectivity.
The present results add a new dimension to the development of synaptic
circuitry in LGN. During early development, retinal fibers from crossed
(contralateral eye) and uncrossed (ipsilateral eye) pathways share common
terminal space in LGN and form functional excitatory and inhibitory
connections. At later ages, starting at the time of eye opening (P14),
synapses between uncrossed retinal axons and relay cells recede, and there is
a loss of binocular responsiveness. That is, ipislateral ON stimulation can no
longer evoke EPSP/IPSP pairs. However, in some cells ipislateral ON
stimulation still evokes IPSP activity. In these instances, synapses between
uncrossed retinal axons and inhibitory LGN interneurons seem to be maintained.
Binocular inhibitory interactions in the adult LGN have been a subject of
intense inquiry, especially in the cat (e.g.,
Guido et al. 1989;
Xue et al. 1987) but also in
the monkey (Schroeder et al.
1990). Typically, these studies involved the use of in vivo
preparations and showed, through extracellular averaging techniques, that
visual stimulation of one (or nondominant) eye had a relatively weak and
varied influence on visual responses activated by the other (or dominant) eye.
Because of this, the actual incidence of binocular inhibitory interactions has
been difficult to ascertain with estimates ranging from 29%
(Guido et al. 1989) to 75%
(Xue et al. 1987). The
circuitry underlying binocular interactions has also been difficult to
delineate. Perhaps the best and most direct evidence for an inhibitory
binocular circuit was detailed by Lindström and colleagues. Using
intracellular recordings in an in vivo cat preparation, a disynaptic,
feed-forward inhibitory circuit was identified
(Lindström 1982). These
feed-forward binocularly mediated IPSPs were shown to arise from separate
interneurons and not from a single one that received convergent retinal input
(Ahlsén et al. 1985). In
the rat, interneurons are dispersed throughout the LGN
(Gabbott et al. 1986) and have
extensive branching patterns that span large regions
(Webster and Rowe 1984;
Zhu and Lo 1999). Thus it is
conceivable that the binocular inhibitory interactions reported here are
consistent with a feed-forward circuit involving interneurons that receive
separate input from the two eyes. Finally their presence in the rodent also
suggests binocular inhibitory circuits in LGN are highly conserved across
mammalian species.
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DISCLOSURES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Present address of J. 
iburkus: George Mason
University, Krasnow Institute for Advanced Study, Mail Stop 2A1, Fairfax, VA
22030.
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FOOTNOTES |
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Address for reprint requests: W. Guido, Dept. of Cell Biology and Anatomy, LSU Health Sciences Center, 1901 Perdido St., New Orleans, LA 70112 (E-mail: WGUIDO{at}LSUHSC.EDU).
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