The Psychiatric Institute, Department of Psychiatry, The University of Illinois at Chicago, Chicago, IL 60612, USA
Address correspondence to J.-M. Mienville, The Psychiatric Institute, Department of Psychiatry; m/c 912, The University of Illinois at Chicago, 1601 West Taylor Street, Chicago, IL 60612, USA. Email: jmm{at}psych.uic.edu.
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Abstract |
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Introduction |
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CajalRetzius (CR) cells represent a major component of layer I in its immature stage. In rodents, they are present in the marginal zone at the earliest stages of neocorticogenesis (Bayer and Altman, 1991), and show time-dependent changes in a number of membrane properties (Fig. 2
) (Zhou and Hablitz, 1996a
; Mienville and Barker, 1997
; Mienville, 1998
; Mienville and Pesold, 1999
; Mienville et al., 1999a
) before disappearing around the end of the second postnatal week (Derer and Derer, 1990
, 1992
; Del Río et al., 1995
, 1996
; Mienville and Pesold, 1999
).
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Some Anatomical and Technical Considerations |
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A morphogenetic role linked to a secretory function has long been suspected for CR cells (Derer and Nakanishi, 1983), but it is not until recently that this role was demonstrated and clearly defined (D'Arcangelo et al., 1995
; Ogawa et al., 1995
) [reviewed by Rakic and Caviness (Rakic and Caviness, 1995
)]. CR cells synthesize and secrete a novel type of extracellular matrix protein necessary for normal lamination of the neocortex. Because the genetic mutation that prevents its expression is responsible for the Reeler phenotype, this protein has been named Reelin. The development of specific antibodies against Reelin (Ogawa et al., 1995
; De Bergeyck et al., 1997
) now provides a further means of identifying CR cells, confirming a posteriori the validity of former criteria based on morphology (Schwartz et al., 1998
; Mienville and Pesold, 1999
).
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Intrinsic Properties of CR Cells |
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Zhou and Hablitz (1996a) were the first to give a substantial electrophysiological account of neocortical CR cells (Zhou and Hablitz, 1996a). [Note, however, that the patch-clamp recordings performed by von Haebler et al. (von Haebler et al., 1993
) in hippocampal horizontal cells, which it seems reasonable to consider as CR cells (Del Río et al., 1996
), may constitute the first account of CR cell physiology.] Their contribution made two important points: (i) the fact that CR cells can fire action potentials (APs) confirmed their neuronal nature [although most glial cells have sodium and potassium voltage-dependent channels, the density ratio of these ion channels is, except for rare cases (Bordey and Sontheimer, 1998
), unfavorable to AP generation (Sontheimer et al., 1996
)] as initially intimated by their selective expression of specific markers (König and Schachner, 1981
); and (ii) in contrast to their early morphological differentiation, CR cells undergo a profound postnatal maturation of their biophysical properties. This second point disproved the common belief that CR cells achieve maturity before birth (Jacobson, 1991
).
The ability to fire APs evokes the possibility of a participation of CR cells in cortical network function. Indirectly supporting this idea, Zhou and Hablitz did not detect any major difference in membrane properties between CR cells and non-CR cells of layer I (Zhou and Hablitz, 1996a). Similarly, Budde and White observed homogeneous properties among CR and non-CR cells acutely dissociated from layer I to record voltage-dependent conductances (Budde and White, 1998
). In this study, however, the actual presence of CR cells may be questioned because the tissue was obtained from rats 36 weeks old, a time when most CR cells have disappeared. At variance with these observations, Hestrin and Armstrong emphasized the longer AP duration and spike train dampening of CR cells compared with other layer I neurons of rat neocortex (Hestrin and Armstrong, 1996
). Likewise, Mienville et al. confirmed the postnatal maturation of CR cell excitability, but underlined the fact that neither AP waveform nor maximal firing frequency appeared compatible with a role in cortical network function (Mienville et al., 1999a
). Such a role is indeed highly unlikely from the simple fact that CR cells disappear before full maturation of the cortex. Finally, a third argument concerns the elusive synaptic connectivity of CR cells. This point along with a possible role for CR cell firing are discussed below.
Another finding was the fact that CR cells display a relatively low resting potential (RP) throughout their life, compared to both other layer I neurons (Mienville, 1998) and layer II/III pyramidal cells (Mienville and Pesold, 1999
). In these studies, instantaneous' RP was measured upon cell break-in, presumably reflecting true RP before whole-cell dialysis. The low RP of CR cells was apparently due to suboptimal activation of the Na/K pump since after 10 min with ATP in the patch electrode RP was restored to a high value (Mienville and Pesold, 1999
). At this point, the mechanisms underlying this low activation may be only speculative; they may pertain either to energy depletion due to various factors, including Reelin synthesis, or to an immature expression of the pump (Haglund et al., 1985
; von Haebler et al., 1993
). Interestingly, a low RP was also found in hippocampal CR cells along with other properties such as low-amplitude, long-duration APs and lack of synaptic input (von Haebler et al., 1993
) that appear characteristic of neocortical CR cells. Regardless, this low RP seems to be determining in the fate of CR cells, as explained below.
Voltage-dependent Conductances
A complete account of voltage-dependent currents in CR cells is not yet available. Nevertheless, the few current-clamp and voltage-clamp experiments that have been performed so far indicate developmental changes, from the late embryonic stage (E18) up to P13, in all the conductances studied. For example, Mienville and Barker did not detect any inward rectifying conductance (IIR) in embryonic CR cells (Mienville and Barker, 1997), whereas current-clamp experiments on early postnatal CR cells revealed hyperpolarization-induced depolarizing sags (Zhou and Hablitz, 1996a
), which is a token of IIR expression. In contrast, from E18 to E21 the proportion of inactivating K current (IA) expressed by CR cells increases (Mienville and Barker, 1997
); however, this trend is reversed in postnatal cells as expression of Kv1.4, the presumed molecular substrate of CR cell IA, and the functional expression of the underlying current both decrease from P1 to P13 (Fig. 2A
), whereas the delayed rectifier K current remains stable (Fig. 2B
) (Mienville et al., 1999a
). It therefore would appear that in these cells IA displays a transient expression that peaks perinatally. The possible relevance of IA's virtual disappearance to CR cell function is discussed later.
No voltage-clamp data are available on sodium or calcium currents in CR cells. Since, however, their APs are blocked by 0.51 µM tetrodotoxin (Zhou and Hablitz, 1996a; Mienville et al., 1999a
), implying sodium channel involvement, one may safely assume that the robust changes observed, from P1 to P13, in various AP parameters (threshold, amplitude, rate of rise, etc.) reflect a commensurate increase in sodium channel density (Zhou and Hablitz, 1996a
; Mienville et al., 1999a
).
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Neurotransmitter Receptors of CR Cells |
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The first electrophysiological recording of a neocortical CR cell seems to be attributable to Kim et al. (Kim et al., 1995) [but see above regarding von Haebler's work (von Haebler et al., 1993
)]. Their work suggested that CR cells express receptors for excitatory amino acids of both the NMDA and non-NMDA type. Although expression of the former has been confirmed thoroughly (Fig. 2C
), responses to AMPA or kainate have been more elusive (Schwartz et al., 1998
; Mienville and Pesold, 1999
). In the central nervous system (CNS), the expression of NMDA receptor subunits is subject to spatiotemporal regulation (Monyer et al., 1994
). In cortex, NR2B subunits are expressed prenatally, whereas NR2A subunits are expressed only postnatally (Sheng et al., 1994
). Our results (Mienville and Pesold, 1999
) suggest that while layer II/III pyramidal neurons may follow this scheme, both embryonic and late postnatal CR cells seem to express a large proportion of NR2B subunits, as if the switch to NR2A expression failed to occur.
Postnatal CR cells incur a dramatic increase in their NMDA receptor density, which ultimately may trigger their death. Thus, a likely scenario is that the low RP of CR cells relieves an increasing density of NMDA channels from magnesium block, leading to overactivation by ambient glutamate (LoTurco et al.,1991; Rakic and Komuro, 1994), calcium overload and subsequent necrosis. This intimates that what takes place is a physiological version of excitotoxicity, which so far has been considered only in a pathological context (McDonald and Johnston, 1990
). The fact that in vivo pharmacological blockade of NMDA receptors curtails the disappearance of CR cells (Mienville and Pesold, 1999
) strongly supports such a hypothesis. Although CR cell RP is intrinsically low, in the sense that in vitro exposure to GABA or NMDA antagonists fails to restore a high RP (Mienville and Pesold, 1999
), it is tempting to speculate that CR cell death results from a cascade that adds insult to injury. That is, in vivo exposure to ambient glutamate (or GABA) probably increases the intrinsic depolarization, there- by providing further relief of NMDA channels from magnesium block. The ensuing calcium overload may then further burden the existing energetic deficit by mobilizing the Na/Ca ATPase, especially if CR cells downregulate their expression of certain calcium-binding proteins (Huntley and Jones, 1990
).
GABAA Receptors
The first demonstration of the presence of GABAA receptors in CR cells should be credited to Schwartz et al. who used a calcium-imaging strategy to simultaneously record a large number of cells in a slice preparation (Schwartz et al., 1998). Their observation that the GABAA agonist muscimol was able to increase intracellular calcium is consistent with the GABAA receptor-mediated depolarization of CR cells (Mienville, 1998
). In the CNS, the developmental switch from a depolarizing to a hyperpolarizing action of GABA has been shown recently to be due to the action of a K+/Cl cotransporter, KCC2, whose expression closely follows patterns of both ontogenetic and phylogenetic maturation (Rivera et al., 1999
). Cells such as dorsal root ganglion neurons, in which the hyperpolarizing switch does not occur, do not express KCC2. As CR cells also fail to activate this switch (Mienville, 1998
), it would be interesting to see if they express KCC2.
Other Receptors
Limited proportions of CR cells have glycine, muscarinic and adrenergic receptors (Schwartz et al., 1998). Non-synaptic, depolarizing glycine receptors (of the strychnine-sensitive type) have been shown to be transiently expressed in perinatal cortex (Flint et al., 1998
), whereas in adult glycine receptors are preferentially expressed in lower brain structures (Cooper et al., 1991
), which may have relevance to CR cell lineage (see below). The responsiveness of CR cells to norepinephrine is interesting in view of the early afferentation of layer I by catecholaminergic fibers (Marín-Padilla, 1998
). Finally, CR cells lack GABAB (Mienville, 1998
) and nicotinic receptors (Schwartz et al., 1998
) (see also J.-M. Mienville, unpublished observations on nicotinic receptors).
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Synaptic Inputs |
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Several Signaling Roles for CR Cells? |
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What, then, could be the purpose of the spontaneous firing of CR cells? No direct answer is presently available, but an exciting and testable hypothesis can be proposed. The formation of neuronal circuits proceeds in three major phases: an initial mapping that relies on chemotactic cues; a structural refinement that depends on spontaneous activity; and a functional refinement that uses sensory experience (Goodman and Shatz, 1993). The differentiation of cortical pyramidal cells includes the elaboration of an apical dendritic arborization anchored in layer I and destined to receive contacts from multiple afferents. CR cells could constitute a temporary interface between these cells and their future afferents (Meyer and González-Hernández, 1993
), for instance by assuring that the formation of active synapses with the apical dendrites of pyramidal neurons allows their vertical elongation (Marín-Padilla, 1998
). Such a role would be reminiscent of that played by subplate neurons in the establishment of thalamocortical projections (Goodman and Shatz, 1993
), with the exception that subplate neurons provide a target for the latter, whereas CR cells would provide an input to pyramids. From this viewpoint, CR cells would be more akin to retinal ganglion cells, whose spontaneously active input to central neurons serves to refine retinofugal connections (Goodman and Shatz, 1993
). The similarity between ganglion cell and CR cell firing frequencies (Galli and Maffei, 1988
; Mienville et al., 1999a
) is compatible with this hypothesis. Ultrastructurally, the latter is also consistent with the finding that CR cell axons make synaptic contacts with pyramidal cell dendrites (Marín-Padilla, 1984
; Del Río et al., 1995
). It is worthwhile noting here the postnatal increase in spontaneous activity and concomitant decline of IA expression in CR cells (Mienville et al., 1999a
). Our computer simulations indicate that both the increase in INa and decrease in IA densities are responsible (and necessary) for repetitive and spontaneous firing to occur, as observed in late CR cells (Mienville et al., 1999b
). A comparable phenomenon was observed in Ascidian embryos, in which the emergence of spontaneous firing is temporally correlated with the disappearance of an inward rectifier potassium current and appearance of a high-threshold calcium current. These two examples thus illustrate possible mechanisms for regulating spontaneous firing as an important developmental function (Moody, 1998
).
There is disagreement as to whether the neurotransmitter synthesized by CR cells is glutamate (Del Río et al., 1995) or GABA (Imamoto et al., 1994
). This would be a relatively trivial issue if depolarization were the only important parameter since both transmitters are depolarizing in immature cortex (Owens et al., 1996
). However, the fact that NMDA receptors, which are abundant in young pyramidal cells (Mienville and Pesold, 1999
), might be involved in activity-dependent circuit maturation (Goodman and Shatz, 1993
) warrants further work to resolve this question. If the above hypothesis was verified, this would imply that CR cells handle two crucial phases of corticogenesis: an early, Reelin-dependent phase concerned with cell placement and perhaps primitive arborization, and a later, activity- dependent phase involving adequate synaptogenesis. [Recently, Borrell et al. also have linked mouse hippocampal CR cells to synaptogenesis, but they implicated Reelin in the underlying mechanism (Borrell et al., 1999
)].
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On the Nature of CR Cells |
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This brings us to the question as to whether these cells are immature forms of neocortical neurons, or whether they could belong to a special class of neurons that happen to settle in the cortex. Marín-Padilla's theory on the dual origin of the mammalian neocortex (Marín-Padilla, 1998) suggests some answers by proposing that layer I phylogenetically and ontogenetically originates from a primitive, pre-mammalian cortex. Being part of layer I, CR cells may thus represent primitive neuronal elements. Interestingly, CR cells seem capable of phylogenetic evolution since they further differentiate into three different subtypes in human cortex (Marín-Padilla, 1984
; Meyer and González- Hernández, 1993
; Meyer et al., 1998
). It would therefore be insightful to investigate whether CR cells recorded from human tissue exhibit distinctive physiological properties, both among themselves and in comparison with those of lower species. A salient feature of CR cells is their limited electrical excitability (Mienville et al., 1999a
), which is probably due to a low sodium channel density; their AP waveform pattern closely resembles that of, for example, astrocytoma (Bordey and Sontheimer, 1998
) or subplate cells (Friauf et al., 1990
). As it turns out, the latter would also be part of the primitive cortex according to the dual-origin theory (Marín-Padilla, 1998
). It is therefore possible that neocortical evolution in mammals endowed layer IIVI cells, along with late-migrating layer I interneurons, with improved ion channel sets that allow ultrafast signaling. As a corollary, CR cells may represent electrically active units in the neuronal circuits of primitive cortices in which lamination is rudimentary (reptiles) or absent (amphibians). This would be consistent with the fact that, contrary to the mammalian case, CR cells persist in large numbers in adult reptilian cortex (Blanton et al., 1987
).
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Concluding Remarks |
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Acknowledgments |
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Footnotes |
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