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Previous Article | Next Article
Volume 16, Number 17, Issue of September 1, 1996 pp. 5290-5300
Copyright ©1996 Society for NeuroscienceMorphology and Physiology of Cortical Neurons in Layer I
Shaul Hestrin1, 2 and William E. Armstrong1 Departments of 1 Anatomy and Neurobiology and 2 Neurology, University of Tennessee, Memphis, Tennessee 38163
ABSTRACT
The electrophysiological and morphological properties of layer I neurons were studied in visual cortex slices from 7- to 19-d-old rats using whole-cell recording and biocytin labeling. A heterogeneous population of small, nonpyramidal neurons was found. Approximately one third of the cells we recorded were neurogliaform cells; another third were multipolar neurons with axons descending out of layer I. The remaining cells were heterogeneous and were not classified. In slices from 7- to 10-d-old animals only, we identified Cajal-Retzius cells.
Neurogliaform neurons had a very dense local axonal field, which was largely contained within layer I. Cells with descending axons had a relatively sparse local axonal arbor and projected at least to layer II and sometimes deeper. Spiking in neurogliaform neurons was followed by an afterdepolarizing potential, whereas spiking in cells with descending axons was followed by a slow after-hyperpolarizing potential (AHP). In addition, neurogliaform cells exhibited less spike broadening and a larger fast AHP after single spikes than did cells with descending axons. Generally, cells in layer I received synaptic inputs characterized as either GABA- or glutamate-mediated, suggesting the presence of excitatory and inhibitory inputs.
With their output largely limited to layer I, neurogliaform cells could synapse with other layer I neurons, the most distal dendritic branches of pyramidal cells, or the dendrites of layer II/III interneurons, which invade layer I. Cells with descending axons could contact a wide variety of cortical cells throughout their vertical projection.
Key words: neurogliaform; Cajal-Retzius; afterdepolarization; afterhyperpolarization; excitation; inhibition
INTRODUCTION
Layer I of the neocortex is relatively cell-sparse and contains mostly nonpyramidal neurons (Prieto et al., 1994). This low density and the location immediately beneath the pial surface has hampered detailed studies of the cellular elements in layer I. In particular, there have been only few studies of layer I neurons using intracellular recordings (Martin et al., 1989
Ramon y Cajal (1911)
MATERIALS AND METHODS
Slice preparation. Parasagittal slices (300 µm thick) from the visual cortex of 7- to 19-d-old rats (Wistar) were obtained using a vibroslicer (Campden). Ice-cold recording solution (see below) was used during slicing. The slices were maintained at 35°C for 1 hr. Slices were kept at room temperature during the recording. The solutions were bubbled with a gas mixture of 95% O2/5% CO2.Recording. Patch pipettes (3-5 M
) were made from thin-wall (1.5 mm outer diameter, 1.17 mm inner diameter) borosilicate glass (Clark) using a vertical electrode puller (PP83, Narishige). Whole-cell recordings (Edwards et al., 1989
10 mV). The voltage and current output were filtered at 1 or 2 kHz (Frequency Devices, Haverhill, MA) and digitized at 12-bit resolution (TL1, Axon Instruments, Foster City, CA). After electrophysiological characterization, the pipette was withdrawn from the cell, and the slice was processed for histology (see below). Miniature excitatory or inhibitory synaptic currents were recorded in the presence of the sodium channel blocker tetrodotoxin (TTX) (Sigma, St. Louis, MO) and detected off-line using a tape storage device (Vetter, Rebersburg, PA). Data were digitized at 10 or 20 KHz and transferred to a disk. Miniature detection was based on threshold crossing of a set amplitude compared with a baseline amplitude. Miniatures were aligned at the 50% amplitude. An exponential function was fitted to each event. The rise times (20-80%), amplitudes, and decay time constants were stored in a separate ascii file used for the construction of histograms.
Solutions. The recording solution contained (in mM): 126 NaCl, 2.5 KCl, 1.25 KH2PO4, 1 MgSO4, 2 CaCl2, 26 NaHCO3, and 10 glucose, pH 7.4 (305 mOsm). Pipettes were filled with a solution containing (in mM): 144 K-gluconate, 3 MgCl2, 10 HEPES, 0.2 EGTA, 4 MgATP, and 0.3 NaGTP, pH 7.2 (295 mOsm). For labeling neurons, biocytin (0.1-0.3%; Sigma) was added to the pipette internal solution. To record miniature inhibitory postsynaptic currents (mIPSCs), we used a chloride-rich internal solution that contained (in mM): 80 K-gluconate, 40 KCl, 10 HEPES, 4 MgATP, 20 creatine phosphate (Na), 0.3 GTP, and 10 EGTA, pH 7.2 (295 mOsm). The AMPA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) (RBI) and the GABA antagonist picrotoxin (RBI) were dissolved in aqueous solution.
Histology. Slices were fixed overnight in a solution of 4% paraformaldehyde, 0.2% picric acid in 0.15 M sodium phosphate buffer (pH 7.2-7.4) at 4°C. After thorough rinsing in PBS, the slices were incubated for 6-18 hr in avidin-biotin-horseradish peroxidase complex (ABC; Vector Labs, Burlingame, CA) in PBS containing 0.5% Triton X-100. The slices were rinsed four times in PBS and then reacted in a solution containing 0.06% 3-3
diaminobenzidine, 0.03% H202, and 0.01-0.05% nickel ammonium sulfate for ~30 min. The slices were then cleared and mounted in a 50-50% solution of glycerol-PBS. The coverslips were sealed with fingernail polish for storage. Filled neurons were drawn with a Nikon Optiphot microscope equipped with a drawing tube. Figures of drawn neurons were created after the drawings were scanned at 300 dpi (Hewlett Packard ScanJet IIcx). Digital micrographs were acquired with a cooled CCD camera (Photometrics, Tucson, AZ) with a frame resolution of 1200 × 1500. Photomontages of individual neurons were created from several focal planes. Final figures were constructed in Adobe Photoshop on a Power Macintosh, where contrast adjustments were made and paste marks removed. Micrographs were printed to a Tektronix Phaser 440 printer at 300 dpi.
Statistics. All error terms listed are SD. Between-group comparisons were made with a two-tailed Mann-Whitney U test.
RESULTS
We were able to recover histologically ~50% of all recorded cells. This article is based on 32 cells that were characterized both morphologically and electrophysiologically. All of the recorded cells could be classified as nonpyramidal neurons, as described earlier (Ramon y Cajal, 1911
Fig. 1. Photomicrographs of layer I biocytin-stained neurons. A, Low-power (A1) and high-power (A2) micrograph of a neurogliaform cell located in the central portion of layer I. The axonal and dendritic arbors are contained within layer I. Note the extensive axonal arborization of this cell type in A2. The arrow points to a varicosity along the axon. B, Low-power (B1) and high-power (B2) micrograph of cell with descending axon (arrowhead) located near the border of layers I and II. Vertical bar delimits layer I. Both dendrites and axons are present in layers I and II. This neuron is drawn in Figure 5. C, Low-power (C1) and high-power (C2) micrograph of a CR cell found close to the pial surface of layer I (9-d-old rat). Both the axon (arrowhead) and the dendrite run parallel to the pial surface. This neuron is drawn in Figure 2. Scale bar in B1 applies to lower-power micrographs; Scale bar in B2 applies to high-power micrographs.
[View Larger Version of this Image (136K GIF file)]
CR cells
CR cells are thought to be the first postmitotic cells that appear during embryonic development (Marin-Padilla, 1984
Fig. 2. The projection tube drawing of a biocytin-stained CR cell (same cell as in Fig. 1) from a 9-d-old animal. The arrowhead indicates the possible site of axon origin. Note the location of the cell in the upper portion of layer I (indicated by the bracket at right of the drawing). Note also the thick single dendrite with small finger-like appendages. Inset, A response to an injection of depolarizing current. Note slow action-potential time course and progressive increase in spike width. Resting potential was
[View Larger Version of this Image (8K GIF file)]
The remaining two CR cells had processes with a similar morphology except that the bipolar orientation was not evident. Regardless, a thin process arose directly from either the soma or a thick process and projected several hundred micrometers beneath the pial surface, branching frequently. All of the CR cells were located in the upper half of layer I. In older rats (11-19 d), we recovered no cells with the unique CR morphology.
The average resting potential of CR cells was
Neurogliaform cells
Eight of the 26 cells we recorded in slices from 11- to 19-d-old rats had a very dense axonal arbor that was contained almost entirely within layer I, and these were characterized as neurogliaform cells (Figs. 1A1,A2, 3). In addition to the dense local axonal arbor, neurogliaform cells had five to six smooth and short primary dendrites that were restricted to layer I, and a small smooth soma (15.7 ± 4.3 × 9.9 ± 1.9 µm). Distally, all of the processes, but particularly the axon, were very thin and required high-magnification, oil-immersion optics to be followed. Neurogliaform cells were typically located in the middle to upper half of layer I. The axonal projection field could extend throughout the dorsoventral extent of the layer and anteroposteriorly 200-300 µm and could fill the thickness of the slice. The density of the arborization and the thinness of the processes often made distinguishing axons from dendrites difficult.
Fig. 3. A projection tube drawing of a biocytin-stained neurogliaform cell in layer I. Borders of layer I are indicated at left of the drawing. The extensive axonal arbor extends close to the border of layer I but does not enter layer II. The central location of the somata is typical of these cells. Inset, A single action potential initiated in this cell by current injection (300 pA, 10 msec) is followed by an afterdepolarization (ADP). Resting potential:
[View Larger Version of this Image (28K GIF file)]
The average resting potential of neurogliaform cells was
Fig. 4. Action-potential characteristics of a neurogliaform cell. All records are from the same cell. A, Steps (900 msec) of current injection (
[View Larger Version of this Image (19K GIF file)]
Fig. 8. AHP and ADP. A, AHP after a single action potential in a cell with a descending axon. Note the PSPs at the end of the voltage trace. Resting potential:
[View Larger Version of this Image (20K GIF file)]
Cells with a descending axon
Seven of the 26 cells from 11- to 19-d-old rats had an axon that descended to layer II or deeper (Figs. 1B1,B2, 5). Like neurogliaform cells, the somata were small (14.9 ± 3.4 × 7.9 ± 1.7 µm) but were typically found in the middle to lower half of layer I. These cells had four to five sparsely branching dendrites. Two of the seven neurons had spiny dendrites, whereas the remaining five were relatively aspiny. For most of these neurons, the dendritic tree extended from the top to the bottom of layer I; additional dendritic projections were commonly found in the upper half of layer II. The anteroposterior extent of dendritic spread, however, was limited to <200 µm from either side of the soma. The distal portions of the dendrites were thin, as were secondary and tertiary branches. The single axon arose from either the soma or a primary dendrite. Although the axon sometimes branched within layer I, the local arborization was sparse when compared with that of neurogliaform cells. Scattered axonal branches were also found in deeper layers, and varicosities were often visible along collateral branches. The axon of two neurons reached layer IV and that of a third reached layer V. The remaining neurons had axons restricted to layers I and II. Collateral branches in deeper layers were not observed to extend anteroposteriorly much beyond ~100 µm from the cell body. The axons were thin distally, however, and the staining was faint, and we cannot rule out a more extensive projection.
Fig. 5. Cell with a descending axon. Soma is located close to layer I-II border (indicated at left of drawing). The axon, whose origin is indicated by arrowhead, descends well into lower layers but gives off a local arbor. Inset, A train of spikes is followed by an afterhyperpolarization (AHP). Resting potential:
[View Larger Version of this Image (13K GIF file)]
The resting potential (
0.02), whereas the action-potential half-width was longer (p
Fig. 6. Action potential characteristics of cells with descending axon. A, Depolarization induced a train of action potentials illustrating spike frequency adaptation. Note the spike broadening during the train. After the train there is an AHP (indicated by filled circle). Resting potential:
[View Larger Version of this Image (21K GIF file)]
Fig. 7. Action potential parameters in neurogliaform cells and cells with descending axons. The fAHP plotted against the half-width of the second spike in a train of spikes. The fAHP of neurogliaform cells (filled symbols) is larger in amplitude than that of cells with descending axons (open symbols). The second spike half-width of the neurogliaform cell is shorter in duration compared with that of cells with descending axons. Inset, Superimposition of the first and second spikes in a train of action potentials. Inset left, Neurogliaform cell; inset right, cell with descending axon.
[View Larger Version of this Image (15K GIF file)]
Other neurons
Three neurons were recovered that had an axon apparently restricted to layer I but did not locally arborize with the density of neurogliaform cells and thus were not classified as such. In addition, some of the dendrites extended into layer II. None of these three cells exhibited an ADP, and only one exhibited the slow AHP characteristic of cells with descending axons. Soma size averaged 16.8 ± 1.4 × 9.1 ± 0.5 µm.The remaining neurons from which we recorded physiological data and recovered a stained neuron were left unclassified because the axon was not well stained. These cells were morphologically and electrophysiologically diverse; two exhibited an ADP and had short dendrites restricted to layer I, reminiscent of neurogliaform cells; five had a slow AHP and longer dendrites that often extended into layer II. Soma size ranged from 15.2 × 2.6 µm for the largest to 10.4 × 7.2 µm for the smallest neuron.
Voltage clamp
The slow time course of the ADP and AHP displayed by the neurogliaform cells and cells with a descending axon, respectively, may reflect slowly relaxing voltage-dependent currents or may be driven by calcium or other second messengers. Under current-clamp conditions, the time course of the ADP or AHP depends on voltage-dependent conductances and the membrane time constant and therefore may not represent the kinetics of the underlying conductance waveform. Figure 8 illustrates AHPs and ADPs in cells with a descending axon (Fig. 8A,C) and in neurogliaform cells (Fig. 8B,D), respectively. Under voltage clamp, a brief membrane depolarization induced a slowly developing outward current in neurons with an AHP (Fig. 8C,C1) and an inward current in cells with an ADP (Fig. 8D,D1). The decays of the I-AHP and I-ADP had a time course of several hundred milliseconds, similar to that of the voltage traces after action potentials. Furthermore, the I-ADP had a clear rising phase, suggesting that this current does not represent a tail current but reflects a slow response to events triggered by brief membrane depolarization.The AHP has been observed in several cell types and is generated by an increase in K-conductance (for review, see Sah, 1996
Fig. 9. Conductance mechanism of the I-ADP. A, The membrane potential was
[View Larger Version of this Image (24K GIF file)]
Excitatory and inhibitory synaptic inputs
Synaptic contacts in layer I of both symmetrical and asymmetrical types have been found (Beaulieu and Colonnier, 1985When the GABAergic blocker picrotoxin (100 µM) was present, the synaptic currents observed at
Fig. 10. mEPSCs and mIPSCs. A1-A3, mEPSCs were detected using a threshold amplitude of
[View Larger Version of this Image (24K GIF file)]
To record IPSCs, we filled the patch pipettes with chloride-rich internal solution (see Materials and Methods). The estimated chloride reversal potential under these conditions is
DISCUSSION
Our main finding is that within layer I, there are distinct groups of small neurons that can be differentiated by their axonal projection and electrophysiological properties. In particular, we identified a group of neurogliaform cells with a very dense axonal field contained within layer I and a second group of neurons with an axon descending to the lower cortical layers. In addition, these two cell types exhibit different electrophysiological properties. Neurogliaform cells and cells with a descending axon are morphologically distinct from the CR cells observed in younger rats.Neurogliaform cells
Neurogliaform cells have been described by several authors (Jones, 1984It has been shown previously that spiking parameters can be used to differentiate pyramidal from nonpyramidal cortical neurons (McCormick et al., 1985
In response to a steady current injection, layer I neurogliaform cells fire action potentials characterized by a large fAHP and less frequency adaptation and spike broadening when compared to cells with descending axons. Spike frequency adaptation and spike broadening are prominent in most pyramidal neurons and are found to a lesser degree in some nonpyramidal cells (Kawaguchi, 1995
Cells with descending axons
We have identified a group of cells that had a prominent descending axon in addition to their local collateral projections. The characteristics of cells with a descending axon have not been studied extensively in the literature; however, Ramon y Cajal (Fig. 54 in DeFelipe and Jones, 1988It is not possible to determine from our material whether the axons extend to the white matter, because the axonal staining became faint distally. Martínez-García et al. (1994)
Cells with a descending axon are clearly differentiated from neurogliaform cells both morphologically and electrophysiologically. Compared with neurogliaform cells, those with a descending axon exhibit a smaller fAHP and a larger spike width. The slow AHP and frequency adaptation seen in cells with a descending axon recall the regular spiking nonpyramidal cells described by Kawaguchi (1995
CR cells
CR cells are among the first postmitotic cells. Recent findings suggest that they are important developmentally (Ogawa et al., 1995Unclassified cells
Our reticence to classify approximately one third of the neurons reflects what we consider to be weak or incomplete staining of axonal arbors. In addition, the morphologies of a few well filled neurons simply could not be generalized to other groups of neurons and stood as isolated examples. It is likely that layer I contains other distinct groups of neurons that we have not identified simply because they were insufficiently represented in our study.Functional implications
The overwhelming majority (90-95%) of neurons in layer I are GABAergic (Gabbott and Somogyi, 1986We found that layer I neurons receive both excitatory and inhibitory synaptic inputs. The excitatory input may be derived from collaterals of local pyramidal neurons and/or extracortical projection, including thalamic fibers. The source of inhibition is probably other neurons in layer I, but axons of inhibitory neurons from the lower layers may also contribute.
The predominant postsynaptic elements within layer I are the distal portions of apical dendrites from pyramidal neurons in layers II-V. Cortical inputs that selectively target layer I may undergo significant electrotonic attenuation (Cauller and Connors, 1994
FOOTNOTES
Received Feb. 20, 1996; revised June 4, 1996; accepted June 5, 1996.
This work was supported by National Eye Institute Grant EY-09120 (S.H.) and National Institutes of Health Grant NS-23941 (W.E.A.). We thank Mario Galarreta and Charlie Wilson for their help, Bob Foehring for comments on this manuscript, and Emin Kuliyev for his excellent technical assistance.
Correspondence should be addressed to Shaul Hestrin, Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, 855 Monroe Avenue, Memphis, TN 38163.
REFERENCES
- Amitai Y, Friedman A, Connors BW, Gutnick MJ (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb Cortex 3:26-38 .
[Abstract/Free Full Text] - Anderson JC, Martin KAC, Picanço-Diniz CW (1992) The neurons in layer 1 of cat visual cortex. Proc R Soc Lond [Biol] 248:27-33 . [Medline]
- Bayer SA, Altman J (1990) Development of layer I and the subplate in the rat neocortex. Exp Neurol 107:48-62 . [Web of Science][Medline]
- Beaulieu C, Colonnier M (1985) A laminar analysis of the number of round-asymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. J Comp Neurol 231:180-189 . [Web of Science][Medline]
- Beaulieu C, Campistron G, Crevier C (1994) Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat. J Comp Neurol 339:559-572 . [Web of Science][Medline]
- Caeser M, Brown DA, Gähwiler BH, Knöpfel T (1993) Characterization of a calcium-dependent current generating a slow afterdepolarization of CA3 pyramidal cells in rat hippocampal slice cultures. Eur J Neurosci 5:560-569 . [Web of Science][Medline]
- Cauller LJ, Connors BW (1994) Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J Neurosci 14:751-762 . [Abstract]
- Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95-116 . [Web of Science][Medline]
- Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99-104 . [Web of Science][Medline]
- Constanti A, Bagetta G, Libri V (1993) Persistent muscarinic excitation in guinea-pig olfactory cortex neurons: involvement of a slow post-stimulus afterdepolarizing current. Neuroscience 56:887-904 . [Web of Science][Medline]
- DeFelipe J, Jones EG (1988) Cajal on the cerebral cortex: an annotated translation of the complete writings. .
- del Rio JA, Martínez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5:13-21 .
[Abstract/Free Full Text] - Derer P, Derer M (1990) Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36:839-856 . [Web of Science][Medline]
- Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflügers Arch 414:600-612 . [Web of Science][Medline]
- Foehring RC, Waters RS (1991) Contributions of low-threshold calcium current and anomalous rectifier (Ih) to slow depolarizations underlying burst firing in human neocortical neurons in vitro. Neurosci Lett 12:17-21.
- Foehring RC, Lorenzon NM, Herron P, Wilson CJ (1991) Correlation of physiologically and morphologically identified neuronal types in human association cortex in vitro. J Neurophysiol 66:1825-1837 .
[Abstract/Free Full Text] - Friedman A, Gutnick MJ (1987) Low-threshold calcium electrogenesis in neocortical neurons. Neurosci Lett 81:117-122 . [Web of Science][Medline]
- Friedman A, Arens J, Heinemann U, Gutnick MJ (1992) Slow depolarizing afterpotentials in neocortical neurons are sodium and calcium dependent. Neurosci Lett 135:13-17 . [Web of Science][Medline]
- Gabbott PL, Somogyi P (1986) Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61:323-331 . [Web of Science][Medline]
- Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204 . [Web of Science][Medline]
- Hablitz JJ, Zhou FM (1995) Dual component mEPSCs in layer I neurons of rat neocortex. Soc Neurosci Abstr 21:2022.
- Hedlich A, Werner L (1987) Neuroglioforme Zellen im visuaellen cortex der ratte. J Hirnforsch 29:107-116.
- Hestrin S (1993) Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 11:1083-1091 . [Web of Science][Medline]
- Huguenard JR, Hamill OP, Prince DA (1989) Sodium channels in dendrites of rat cortical pyramidal neurons. Proc Natl Acad Sci USA 86:2473-2477 .
[Abstract/Free Full Text] - Huntley GW, Jones EG (1990) Cajal-Retzius neurons in developing monkey neocortex show immunoreactivity for calcium binding proteins. J Neurocytol 19:200-212 . [Web of Science][Medline]
- Jones EG (1984) Neurogliaform or spiderweb cells. In: Cerebral cortex (Peters, A, Jones, E, eds) , p. 409. New York: Plenum.
- Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H (1994) Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281-1289 . [Web of Science][Medline]
- Kawaguchi Y (1993) Grouping of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69:416-431 .
[Abstract/Free Full Text] - Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655 . [Abstract]
- Kawaguchi Y (1996) Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16:2701-2715.
[Abstract/Free Full Text] - Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396 .
[Abstract/Free Full Text] - Kim HG, Connors BW (1993) Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13:5301-5311 . [Abstract]
- Kim HG, Fox K, Connors BW (1995) Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. Cereb Cortex 5:148-157 .
[Abstract/Free Full Text] - Kriegstein AR, Suppes T, Prince DA (1987) Cellular and synaptic physiology and epileptogenesis of developing rat neocortical neurons in vitro. Dev Brain Res 34:161-171.
- Lambolez B, Ropert N, Perrais D, Rossier J, Hestrin S (1996) Correlation between kinetics and RNA splicing of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in neocortical neurons. Proc Natl Acad Sci USA 93:1797-1802.
[Abstract/Free Full Text] - Li J, Schwark HD (1994) Distribution and proportions of GABA-immunoreactive neurons in cat primary somatosensory cortex. J Comp Neurol 343:353-361 . [Web of Science][Medline]
- Lorenzon NM, Foehring RC (1993) The ontogeny of repetitive firing and its modulation by norepinephrine in rat neocortical neurons. Dev Brain Res 73:213-223 . [Medline]
- Magee JC, Christofi G, Miyakawa H, Christie B, Lasser-Ross N, Johnston D (1995) Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. J Neurophysiol 74:1335-1342 .
[Abstract/Free Full Text] - Marin-Padilla M (1984) Neurons of layer I: a developmental analysis. In: Cerebral cortex (Peters, A, Jones, EG, eds) , p. 447. New York: Plenum.
- Martin KAC, Friedlander MJ, Alones V (1989) Physiological, morphological, and cytochemical characteristics of a layer 1 neuron in cat striate cortex. J Comp Neurol 282:404-414. [Web of Science][Medline]
- Martínez-García F, Gonzalez-Hernandez T, Martínez-Millan L (1994) Pyramidal and nonpyramidal callosal cells in the striate cortex of the adult rat. J Comp Neurol 350:439-451.[Web of Science][Medline]
- McCormick DA, Prince DA (1987) Post-natal development of electrophysiological properties of rat cerebral pyramidal neurones. J Physiol (Lond) 392:743-762.
- McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806 .
[Abstract/Free Full Text] - Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912 . [Web of Science][Medline]
- Pockberger H (1991) Electrophysiological and morphological properties of rat motor cortex neurons in vivo. Brain Res 539:181-190 . [Web of Science][Medline]
- Prieto JJ, Peterson BA, Winer JA (1994) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J Comp Neurol 344:349-382 . [Web of Science][Medline]
- Ramon y Cajal S (1911) Histologie du System Nerveux de l'Homme et des Vertebrates. (Translated into English by N Swanson and LW Swanson as Histology of the Nervous System of Man and Vertebrates.) 1995.
- Sah P (1996) Ca2+-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci 19:150-154 . [Web of Science][Medline]
- Schwindt PC, Crill WE (1995) Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74:2220-2224 .
[Abstract/Free Full Text] - Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450-467 .
[Abstract/Free Full Text] - Sousa-Pinto A, Paula-Barbosa M, Carmo-Matos M (1975) A Golgi and electron microscopical study of nerve cells in layer I of the cat auditory cortex. Brain Res 95:443-458 . [Web of Science][Medline]
- Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15:1065-1076 . [Web of Science][Medline]
- Winer JA, Larue DT (1989) Populations of GABAergic neurons and axons in layer I of rat auditory cortex. Neuroscience 33:499-515 . [Web of Science][Medline]
- Zhou F-M, Hablitz JJ (1996) Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16:1131-1139 .
[Abstract/Free Full Text]
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K. Kirmse, A. Dvorzhak, R. Grantyn, and S. Kirischuk
Developmental Downregulation of Excitatory GABAergic Transmission in Neocortical Layer I via Presynaptic Adenosine A1 Receptors
Cereb Cortex, February 1, 2008; 18(2): 424 - 432.
[Abstract] [Full Text] [PDF]
K. Kirmse, A. Dvorzhak, C. Henneberger, R. Grantyn, and S. Kirischuk
Cajal Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs
J. Physiol., December 15, 2007; 585(3): 881 - 895.
[Abstract] [Full Text] [PDF]
N. V. Povysheva, A. V. Zaitsev, S. Kroner, O. A. Krimer, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer
Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex
J Neurophysiol, February 1, 2007; 97(2): 1030 - 1039.
[Abstract] [Full Text] [PDF]
D. Shlosberg, Y. Amitai, and R. Azouz
Time-Dependent, Layer-Specific Modulation of Sensory Responses Mediated by Neocortical Layer 1
J Neurophysiol, December 1, 2006; 96(6): 3170 - 3182.
[Abstract] [Full Text] [PDF]
Z. Chu and S. M. Moenter
Physiologic Regulation of a Tetrodotoxin-Sensitive Sodium Influx That Mediates a Slow Afterdepolarization Potential in Gonadotropin-Releasing Hormone Neurons: Possible Implications for the Central Regulation of Fertility.
J. Neurosci., November 15, 2006; 26(46): 11961 - 11973.
[Abstract] [Full Text] [PDF]
K. Kirmse and S. Kirischuk
Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex.
J. Neurosci., April 19, 2006; 26(16): 4216 - 4227.
[Abstract] [Full Text] [PDF]
V. Zsiros and G. Maccaferri
Electrical Coupling between Interneurons with Different Excitable Properties in the Stratum Lacunosum-Moleculare of the Juvenile CA1 Rat Hippocampus
J. Neurosci., September 21, 2005; 25(38): 8686 - 8695.
[Abstract] [Full Text] [PDF]
C. J. Price, B. Cauli, E. R. Kovacs, A. Kulik, B. Lambolez, R. Shigemoto, and M. Capogna
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
J. Neurosci., July 20, 2005; 25(29): 6775 - 6786.
[Abstract] [Full Text] [PDF]
A. Simon, S. Olah, G. Molnar, J. Szabadics, and G. Tamas
Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex
J. Neurosci., July 6, 2005; 25(27): 6278 - 6285.
[Abstract] [Full Text] [PDF]
J. Wu and J. J. Hablitz
Cooperative Activation of D1 and D2 Dopamine Receptors Enhances a Hyperpolarization-Activated Inward Current in Layer I Interneurons
J. Neurosci., July 6, 2005; 25(27): 6322 - 6328.
[Abstract] [Full Text] [PDF]
E. B. Merriam, T. I. Netoff, and M. I. Banks
Bistable Network Behavior of Layer I Interneurons in Auditory Cortex
J. Neurosci., June 29, 2005; 25(26): 6175 - 6186.
[Abstract] [Full Text] [PDF]
M. J. Higley and D. Contreras
Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo
J Neurophysiol, April 1, 2005; 93(4): 1920 - 1934.
[Abstract] [Full Text] [PDF]
Y. Zhu and J. J. Zhu
Rapid Arrival and Integration of Ascending Sensory Information in Layer 1 Nonpyramidal Neurons and Tuft Dendrites of Layer 5 Pyramidal Neurons of the Neocortex
J. Neurosci., February 11, 2004; 24(6): 1272 - 1279.
[Abstract] [Full Text] [PDF]
Y. Gonchar and A. Burkhalter
Distinct GABAergic Targets of Feedforward and Feedback Connections Between Lower and Higher Areas of Rat Visual Cortex
J. Neurosci., November 26, 2003; 23(34): 10904 - 10912.
[Abstract] [Full Text] [PDF]
T. Soda, R. Nakashima, D. Watanabe, K. Nakajima, I. Pastan, and S. Nakanishi
Segregation and Coactivation of Developing Neocortical Layer 1 Neurons
J. Neurosci., July 16, 2003; 23(15): 6272 - 6279.
[Abstract] [Full Text] [PDF]
G. Tamas, A. L. A. Simon, and J. Szabadics
Identified Sources and Targets of Slow Inhibition in the Neocortex
Science, March 21, 2003; 299(5614): 1902 - 1905.
[Abstract] [Full Text] [PDF]
L. G. Nowak, R. Azouz, M. V. Sanchez-Vives, C. M. Gray, and D. A. McCormick
Electrophysiological Classes of Cat Primary Visual Cortical Neurons In Vivo as Revealed by Quantitative Analyses
J Neurophysiol, March 1, 2003; 89(3): 1541 - 1566.
[Abstract] [Full Text] [PDF]
Z. Chu, M. Galarreta, and S. Hestrin
Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1
J. Neurosci., January 1, 2003; 23(1): 96 - 102.
[Abstract] [Full Text] [PDF]
R. C. Foehring, J. F. M. van Brederode, G. A. Kinney, and W. J. Spain
Serotonergic Modulation of Supragranular Neurons in Rat Sensorimotor Cortex
J. Neurosci., September 15, 2002; 22(18): 8238 - 8250.
[Abstract] [Full Text] [PDF]
E. Christophe, A. Roebuck, J. F. Staiger, D. J. Lavery, S. Charpak, and E. Audinat
Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
J Neurophysiol, September 1, 2002; 88(3): 1318 - 1327.
[Abstract] [Full Text] [PDF]
G. Radnikow, D. Feldmeyer, and J. Lubke
Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal-Retzius Cells in the Developing Rat Neocortex
J. Neurosci., August 15, 2002; 22(16): 6908 - 6919.
[Abstract] [Full Text] [PDF]
A. Peters and C. Sethares
The Effects of Age on the Cells in Layer 1 of Primate Cerebral Cortex
Cereb Cortex, January 1, 2002; 12(1): 27 - 36.
[Abstract] [Full Text] [PDF]
W. Kilb and H. J. Luhmann
Characterization of a Hyperpolarization-Activated Inward Current in Cajal-Retzius Cells in Rat Neonatal Neocortex
J Neurophysiol, September 1, 2000; 84(3): 1681 - 1691.
[Abstract] [Full Text] [PDF]
R. S. Dammerman, A. C. Flint, S. Noctor, and A. R. Kriegstein
An Excitatory GABAergic Plexus in Developing Neocortical Layer 1
J Neurophysiol, July 1, 2000; 84(1): 428 - 434.
[Abstract] [Full Text] [PDF]
A. Aguilo, T. H. Schwartz, V. S. Kumar, Z. A. Peterlin, A. Tsiola, E. Soriano, and R. Yuste
Involvement of Cajal-Retzius Neurons in Spontaneous Correlated Activity of Embryonic and Postnatal Layer 1 from Wild-Type and Reeler Mice
J. Neurosci., December 15, 1999; 19(24): 10856 - 10868.
[Abstract] [Full Text] [PDF]
J.-M. Mienville
Feature Article: Cajal-Retzius Cell Physiology: Just in Time to Bridge the 20th Century
Cereb Cortex, December 1, 1999; 9(8): 776 - 782.
[Abstract] [Full Text] [PDF]
J.-M. Mienville, I. Maric, D. Maric, and J. R. Clay
Loss of IA Expression and Increased Excitability in Postnatal Rat Cajal-Retzius Cells
J Neurophysiol, September 1, 1999; 82(3): 1303 - 1310.
[Abstract] [Full Text] [PDF]
K. R. Alper
The EEG and Cocaine Sensitization: A Hypothesis
J Neuropsychiatry Clin Neurosci, May 1, 1999; 11(2): 209 - 221.
[Abstract] [Full Text]
J.-M. Mienville and C. Pesold
Low Resting Potential and Postnatal Upregulation of NMDA Receptors May Cause Cajal-Retzius Cell Death
J. Neurosci., March 1, 1999; 19(5): 1636 - 1646.
[Abstract] [Full Text] [PDF]
J.-M. Mienville
Persistent depolarizing action of GABA in rat Cajal-Retzius cells
J. Physiol., November 1, 1998; 512(3): 809 - 817.
[Abstract] [Full Text] [PDF]
K. Ceranik, R. Bender, J. R. P. Geiger, H. Monyer, P. Jonas, M. Frotscher, and J. Lubke
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
J. Neurosci., July 15, 1997; 17(14): 5380 - 5394.
[Abstract] [Full Text] [PDF]
E. S. Fortune and G. J. Rose
Passive and Active Membrane Properties Contribute to the Temporal Filtering Properties of Midbrain Neurons In Vivo
J. Neurosci., May 15, 1997; 17(10): 3815 - 3825.
[Abstract] [Full Text] [PDF]
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