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Previous Article | Next Article
The Journal of Neuroscience, November 15, 1998, 18(22):9354-9364
Development of Functional Topography in the Corticorubral Projection: An In Vivo Assessment Using Synaptic Potentials Recorded from Fetal and Newborn Cats
Wen-Jie Song and Fujio Murakami Division of Biophysical Engineering, Graduate School of Engineering Science, Osaka University, Toyonaka 560, Japan
ABSTRACT
Top
Abstract
Introduction
In mammals, topographic maps emerge from initially diffuse projections during development. To gain insight into the mechanisms governing the transition from a diffuse projection to a topographic map, we studied topographic specificity of functional connections during development, using the cat corticorubral system as a model. In the adult cat, rubrospinal neurons in the dorsomedial part of the red nucleus (RN) receive input primarily from the forelimb area of the sensorimotor cortex, whereas those in the ventrolateral part receive input primarily from the hindlimb area. During development, axons from the sensorimotor cortex arrive in the RN at embryonic day 50 (E50) (Song et al., 1995a
) and are diffusely distributed in the RN until postnatal day 13 (P13) (Higashi et al., 1990
Key words: topographic map; sensorimotor cortex; red nucleus; rubrospinal neuron; immature synapse; intracellular recording
INTRODUCTION
Topographic organization in neuronal connections provides a structural basis for parallel processing in the brain. The development of topographic maps, therefore, has been a subject of intense research (for review, see Udin and Fawcett, 1988
This issue has been extensively studied in the retinotectal projections of fish and amphibians. In these species, retinal axons are guided or restricted to the topographically correct tectal regions without errors from the outset of innervation (Sakaguchi and Murphey, 1985
Studies of the rodent retinocollicular projection, however, suggest that a different cellular mechanism operates for the formation of topography; retinal neurons initially send diffuse projections to the superior colliculus, and the topographic map is formed only thereafter (Simon and O'Leary, 1992a
We have examined the perinatal development of topographic specificity of "functional" connections, or functional topography, in the corticorubral system of the cat, using intracellularly recorded synaptic potentials. The corticorubral system of the cat is also organized in a topographic manner; rubrospinal neurons in the dorsomedial part of the red nucleus (RN) receive inputs primarily from the forelimb area of the sensorimotor cortex, innervating the cervicothoracic cord, whereas those in the ventrolateral part receive inputs primarily from the hindlimb area, projecting to the lumbosacral cord (see Fig. 1A) (Pompeiano and Brodal, 1957
The results presented here show that the adult-like functional topographic map in the corticorubral projection is not formed before birth, suggesting that cortical axons initially make functional synapses nonselectively with rubrospinal neurons. The functional topographic map, however, was found to be formed in postnatal cats before the emergence of a clear anatomical map.
MATERIALS AND METHODS
Animals. Five preterm and 36 postnatal cats aged E61 to P28 were used. All animals were raised in a breeding colony of Aburahi Labs of Shionogi & Co., Ltd. Gestation period was 67 d on average. Mating was allowed for 12 hr, and the time of mating was counted as E0. For postnatal cats, the day of birth was counted as P0.
Surgery. All experiments were conducted in compliance with the Guidelines for Use of Laboratory Animals of Osaka University. Cats were anesthetized with initial doses of sodium pentobarbitone (Nembutal) of 25-30 mg/kg (i.p.). Supplementary doses of Nembutal (2-4 mg/kg/hr, i.v.) were given regularly during surgery and recording to maintain anesthesia. Gallamine triethiodide (20 mg/kg/hr, i.v.) was applied to paralyze the animal during recording. The adequacy of anesthesia was judged by the absence of reflexes to ear and toe pinches before paralyzation. The procedures for delivery of the fetuses, fixation of the animal to the stereotaxic frame, and other procedures have been described previously in detail (Song et al., 1995b
Stimulation and intracellular recording. The experimental arrangement is diagrammed in Figure 1, B and C. The RN was located by recording orthodromic field potentials evoked by activation of the contralateral cerebellar nuclei (CN) (Song et al., 1993
To assess the functional topography of the corticorubral projection, the sensorimotor cortex ipsilateral to the recorded RN was stimulated at four sites at the same strength (see Fig. 1C). The same type of bipolar electrodes as for the CN were used for stimulation of the sensorimotor cortex. The bipolar electrodes were lined perpendicularly to the cruciate sulcus and were set to straddle the sulcus to minimize mediolateral spread of stimulation currents. To compensate for developmental change of brain size, the length (L) of the cruciate sulcus was measured first. This length ranged from 1.7 mm to 5.8 mm, depending on age. The third pair of electrodes from the midline was always set at the lateral end of the sulcus; the distance between pairs of electrodes was set at (2.3/5)L. By this method, the medial two pairs of electrodes were placed in the hindlimb region, and the lateral two were placed in the forelimb region (Rubel, 1971
resistor connected to the stimulation circuit in series. The current did not vary substantially among electrodes (<2%). Because cortical efferent neurons are distributed in a sheet, relatively strong stimulus strength was required to evoke a corticorubral response. The topography was estimated using stimulus strength of 30-100 V, corresponding to currents of 130-1000 µA. A wider range of 10-120 V was used to examine synaptic potentials.
The method of intracellular recording has been described previously (Song et al., 1995b
Intracellular injection of biocytin. Biocytin was injected intracellularly after recording in 14 cells to verify that recorded cells were in fact RN neurons. The methods for injection and visualization of biocytin followed Song et al. (1993)
Wheat germ agglutinin-horseradish peroxidase injection. To study the topography of the rubrospinal projection in fetal cats, wheat germ agglutinin-horseradish peroxidase (WGA-HRP) (2% in saline, 0.1 µl; Toyobo) was injected into the L1 segment with a Hamilton syringe, under the anesthesia specified above. After 2 d, the fetus was perfused under deep anesthesia with 1.25% glutaraldehyde and 1% paraformaldehyde in phosphate buffer. The brainstem was sectioned into 70-µm-thick sections and processed for visualization of WGA-HRP using tetramethyl benzidine as the chromogen. Labeled cell bodies were marked on a drawing paper with a drawing tube attached to a light microscope.
Ibotenic acid injection. To verify that corticorubral cells are responsible for synaptic potentials evoked in rubrospinal neurons by stimulation of the sensorimotor cortex, cortical neurons were selectively destroyed by ibotenic acid injection (Schwarcz et al., 1979
Histology. After electrophysiological experiments, the loci of stimulating electrodes in the CN were marked by passing negative current (0.4 mA, 5 sec), and the animal was perfused with 3.5% formaldehyde under deep anesthesia. Recording electrode tracks and stimulating electrode loci were verified in Nissl-stained sections.
Statistical analyses. The functional topography in the corticorubral projection was assessed in individual rubrospinal neurons and was classified either as adult-like or nonadult-like. The occurrence of cells with adult-like topography should then follow the binomial rule. With a sufficiently large number of cells, the binomial distribution approximates a normal distribution (Soeda et al., 1980
np)/(np(1
RESULTS
Topography in rubrospinal projections of preterm kittens
Because rubrospinal neurons in the dorsomedial part of the RN project to the cervicothoracic cord and those in the ventrolateral part innervate the lumbosacral cord (Pompeiano and Brodal, 1957
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Figure 1. Topographic map of the corticorubrospinal system of adult cat and the experimental arrangement for studying the development of the topography. A, A schematic depiction of the topography in adult cat. The forelimb area of the sensorimotor cortex, i.e., the lateral posterior sigmoid gyrus (LPSG), projects to the dorsomedial portion of the RN, which innervates the cervicothoracic cord. The hindlimb cortical area, the medial posterior sigmoid gyrus (MPSG), projects to the ventrolateral portion of the RN, which innervates the lower cord. Rubrospinal cells in dorsomedial and ventrolateral portions of the RN are called C-cells and L-cells, respectively. B, The experimental arrangement. The RN was identified by stereotaxic coordinates and field potentials evoked by stimulation of the contralateral deep CN. Rubrospinal neurons were identified either as a C-cell or an L-cell by their responses to stimulation of the first cervical segment (C1) and the first lumbar segment (L1). Synaptic potentials evoked by stimulation of different sites in the cortex were recorded intracellularly from rubrospinal neurons to assess the pattern of functional input from the cortex to the recorded neuron. C, A dorsal view of the cortex showing the locations of the stimulating electrodes in the sensorimotor cortex. Bipolar stimulating electrodes were set at four sites for postnatal kittens and two for fetal cats. The medial two pairs of electrodes were set in the hindlimb region, and the lateral two pairs were set in the forelimb region. See Materials and Methods for details. All pairs of the bipolar stimulating electrode were lined perpendicularly to the cruciate sulcus (CS) and were set to straddle the sulcus to minimize current spread to neighboring sites.
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Figure 2. The topography of rubrospinal projection in fetal cats. The distribution of rubrospinal neurons retrogradely labeled by injection of WGA-HRP into the first lumbar segment in an E61 kitten. Each circle represents a labeled cell body, and the broken line approximates the border of the RN. The third, the fifth, and the seventh sections of eight horizontal sections, counting from dorsal end of the RN, are lined from left to right. Note the strict localization of labeled neurons to the ventrolateral portion of the RN.
Intracellular staining of electrophysiologically identified rubrospinal neurons revealed that all C-cells (n = 6; one from an E62 fetus) were in the dorsomedial portion of the RN, and all L-cells (n = 8) were in the ventrolateral portion (data not shown).
Together, the above results suggest that an adult-like topographic map is established before E61 in the feline rubrospinal system.
Synaptic potentials evoked by cortical stimulation in preterm and postnatal rubrospinal neurons
Having demonstrated that the topography in the rubrospinal projection is established before E61, the location of rubrospinal neurons within the RN of developing cats could be inferred from their antidromic responses to stimulation of the spinal cord. Thus, by examining the responses to stimulation of different cortical sites in antidromically identified rubrospinal neurons, we were able to study the functional topography in the corticorubral system.
The results described in this and the following sections were obtained from 128 rubrospinal neurons, identified by their antidromic responses to stimulation of C1 and L1 spinal segments. These neurons had resting membrane potentials more negative than -50 mV, and the fluctuation of resting membrane potential was less than ±2.5 mV during recording. Antidromic action potentials were identified according to previously described criteria (Song et al., 1995b
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Figure 3. Synaptic potentials evoked in rubrospinal neurons by stimulation of the sensorimotor cortex in perinatal kittens. A, Top two traces, Antidromic responses evoked in an E62 neuron. Such antidromic spikes were used for identification of rubrospinal neurons as C-cells or L-cells. Traces three to five are examples of synaptic potentials evoked in an E62 fetus, a P13 kitten, and a P28 kitten, respectively. The corresponding stimulus strengths are 80 V, 40 V, and 40 V, respectively. B, Plot of the amplitude of EPSPs evoked by a 50 V stimulating pulse as a function of postnatal days (n = 56). C, Plot of the stimulus strength required for evoking an EPSP with an amplitude of 1.2 ± 0.2 mV as a function of postnatal days (n = 15). D, Plot of the latency of the EPSPs as a function of age. The latency of all EPSPs evoked from topographically appropriate cortical sites in 128 recorded neurons was plotted. The latency of EPSPs having slow rise from the baseline was difficult to determine and was excluded.
The cruciate sulcus is recognizable from E53 in the cat (Song et al., 1995a
Increasing the strength of stimulation at topographically appropriate cortical sites elicited action potentials at the EPSP peaks in postnatal kittens but never in the preterm kittens. The amplitude of EPSPs evoked with a fixed stimulus strength increased with age (Fig. 3B). Provided that the EPSPs were monosynaptic and of cortical origin, these results suggest that the cortical input from topographically appropriate sites to the RN increases over the perinatal period. Consistent with this notion, the stimulus strength required to evoke an EPSP of fixed amplitude appeared to decrease with age (Fig. 3C).
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Figure 4. Synaptic potentials evoked by stimulation of the cortex are of cortical origin and are homogeneous up to the peak. A, Destruction of cortical neurons eliminated the potentials evoked by cortical stimulation. The figure to the right in the inset depicts the surface view of the pericruciate cortex in which ibotenic acid had been injected in a P4 kitten (injection sites marked by the circles). The rest of the inset figures are drawings of parasagittal sections of the cortex, whose positions are like-labeled in the right figure. Shaded area indicates the area of cortical destruction. Stimulation of such cortical areas at 120 V evoked no response in rubrospinal neurons (top trace), although in the same cell, both EPSPs and action potentials could be evoked by stimulation of the CN (bottom trace, white arrow points to the EPSP; stimulus strength = 40 V). Recordings from a P8 kitten. CS, Cruciate sulcus. B, Synaptic potentials evoked by stimulation of the cortex were depressed by intravenous successive application of pentobarbital (top three traces). At the bottom, all three traces were superimposed, with their amplitudes normalized to that of the control, showing the absence of change in shape for potentials from the onset to the peak. All traces are the average of five consecutive recordings from a cell in a P8 kitten. Stimulus strength was 60 V.
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Figure 5. Functional topography of the corticorubral projection in postnatal kittens. A1, The cortical input pattern in an L-cell of a P13 kitten. The cell responded to stimulation of the medial part of the postcruciate gyrus with EPSPs of the largest amplitude, demonstrating that the topographic arrangement in this cell is adult-like. A2, An adult-like L-cell of a P6 kitten. Action potentials were evoked in the top trace but were crippled. A3, An example of an L-cell showing nonadult-like topography in a P6 kitten. B1, A C-cell showing adult-like topography in a P27 kitten. B2, A C-cell showing adult-like topography in a P4 kitten. B3, A C-cell showing nonadult-like topography in a P2 kitten. Stimulus strength was 40 V for B2 and 60 V for the rest. All recordings are superpositions of two to five traces. CS, Cruciate sulcus. Scale bars in the insets apply only to the cruciate sulcus. The white circles approximate the positions of stimulation site in the cortex. Arrowheads mark the timing of stimulation.
The EPSPs evoked by cortical stimulation appear to be monosynaptic
It is most likely that the EPSPs were elicited by activation of efferent neurons in the sensorimotor cortex rather than passing axons. To verify this point, we selectively destroyed cortical neurons by injecting ibotenic acid into the sensorimotor area. Ibotenic acid selectively destroys cell bodies but leaves axons of passage undamaged, presumably by activating glutamate receptors (Schwarcz et al., 1979
The above experiment, however, does not exclude the possibility that the EPSPs recorded in rubrospinal neurons were elicited polysynaptically. To address this possibility, we first measured the EPSP latencies, defined as the time interval from the stimulus artifact to the time when the potential deflects from the baseline. Although the latency of the EPSPs was longer than that in adults, it did not fluctuate measurably over repeated trials of stimulation. The latencies of all EPSPs are plotted as a function of age in Figure 3D. These latencies are comparable to the conduction times of kitten cortical axons from the cortex to the trapezoid body, at corresponding ages (Oka et al., 1985
The EPSPs recorded are the temporal and spatial summation of unitary EPSPs of varying latencies (Fig. 3A). The latency of such compound EPSPs should reflect the conduction of the fastest axons activated by cortical stimulation. Therefore, the fact that the latency of compound EPSPs coincides with the cortical axonal conduction time does not necessarily indicate that the entire EPSP is monosynaptic. To address this issue, we studied the effect of pentobarbital. In addition to potentiating GABAA receptor function, the general anesthetic pentobarbital is also known to suppress excitatory synaptic transmission (Hubbard et al., 1969
Together, the results described in this section suggest that, under deep anesthesia, stimulation of the sensorimotor cortex evokes monosynaptic EPSPs in rubrospinal neurons of kittens. The amplitude of the EPSPs recorded in rubrospinal neurons thus should reflect the amount of input from the stimulated cortical site.
The pattern of corticorubral connections in postnatal kittens resembles the adult pattern
The functional topography in the corticorubral projection was thus examined by comparing the amplitude of the EPSPs evoked from the forelimb and the hindlimb areas of the cortex in individual rubrospinal neurons (C-cells and L-cells; see Results, Topography in rubrospinal projections of preterm kittens). In adult cats, L-cells receive input predominantly from the hindlimb cortical region, whereas C-cells receive input primarily from the forelimb region (Tsukahara and Kosaka, 1968
In P13-P28 kittens, adult-like topography was observed in 33 of 35 recorded L-cells (94%) and in six of seven recorded C-cells (86%). Although there appeared to be a sampling bias toward L-cells, there was no significant difference in the proportion of cells showing adult-like topography between C-cells and L-cells (p > 0.4). We thus pooled the results of C-cells and L-cells together. In P13-P28 kittens, 93% (39 of 42) of recorded rubrospinal neurons showed adult-like functional topography (Fig. 6).
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Figure 6. Percentage of neurons exhibiting adult-like functional topography in three groups of different ages. With increasing age, a larger percentage of neurons showed adult-like functional topography. Numbers in parentheses represent the sample size (n) for each group. The percentages of the P1-P8 and P13-P28 groups are significantly >50% (p < 0.002), whereas the percentage of the E61-E65 group is not (p > 0.4).
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Figure 7. Functional topography of the corticorubral projection in fetal cats. A, The responses of an L-cell in an E62 fetus to stimulation of the two cortical sites are shown as the top two traces. This cell was classified as adult-like, because the response evoked from the hindlimb region was larger. Stimulus strength was 80 V. The trace labeled as (3) is the response evoked by simultaneous stimulation of both cortical sites. At the bottom, this recording was superimposed to the sum of the EPSPs evoked by stimulation of each of the two sites. The slightly larger amplitude of the (3) recording than that of the sum suggests that the stimulation to the two sites overlapped only at subthreshold level. B, An example of an L-cell showing nonadult-like topography in an E62 fetus. Stimulus strength was 50 V. All traces are averages of three consecutive recordings. CS, Cruciate sulcus. Scale bars in the insets apply only to the cruciate sulcus. Calibration in B also applies to A.
In P1-P8 kittens, cells showing adult-like topography constituted 82% of the total (n = 56; C-cell, 9 of 11; L-cell, 37 of 45) (Fig. 6). This percentage was not significantly different from that of the P13-P28 kittens (p > 0.1). For both groups, the percentages cannot be expected from a random corticorubral connection (p < 0.002), in which case the probability of observing adult-like cells would be 50%. These results suggest that the functional topography in the corticorubral system is present in the first postnatal week.
Corticorubral connection in preterm kittens is diffuse
The small-sized brain of preterm kittens allowed us to set stimulating electrodes at only two sites in the cortex (see Materials and Methods). In all preterm kittens, stimulation of either site evoked responses of similar amplitudes in rubrospinal cells, as exemplified in Figure 7. The topography of each cell was nevertheless classified either as adult-like or nonadult-like, following the definition described above. The L-cell shown in Figure 7A, for example, was classified as a cell showing adult-like topography, because the amplitude of the EPSP evoked from the hindlimb region was slightly larger; the L-cell shown in Figure 7B was classified as nonadult-like, because the amplitude of the EPSP evoked from the hindlimb region was smaller. In contrast to postnatal kittens, of all 22 rubrospinal neurons recorded in E61-E65 preterm kittens, only 41% showed adult-like functional topography (C-cell, 2/4; L-cell, 7/18) (Fig. 6). This percentage is not significantly different from the probability of 0.5 (p > 0.4), which would be expected if the corticorubral innervation were random. These results suggest that the functional corticorubral connection in preterm kittens is diffuse.
The result that the amplitudes of the EPSPs evoked from the two stimulation sites were comparable raises the possibility that the stimulation current had spread to the neighboring stimulation site so that both electrodes stimulated an overlapping population of efferent neurons. To test this, both sites were stimulated simultaneously with the same strength as the case when each site was stimulated alone (Fig. 7A). The amplitude of EPSPs evoked in this manner was close to the summation of the EPSPs evoked from each of the two sites (Fig. 7A, bottom panel), suggesting that the response evoked from each site primarily reflects the cortical input from that site. Similar results were obtained in all tested cells in prenatal (n = 5) and postnatal kittens (n = 8) with subthreshold stimulation.
Because the corticorubral projection in preterm kittens was assessed with two pairs of electrodes and that in postnatal kittens was done with four pairs, the difference in the observed pattern of connection between the two groups could have been attributable to the methodological difference. To address this possibility, three P5-P7 kittens were studied with two pairs of stimulating electrodes, set in the same manner as in the preterm kittens. Seven of eight neurons (87.5%) recorded from these kittens showed adult-like functional topography, a result comparable to that obtained with four pairs of electrodes in P1-P8 kittens.
DISCUSSION
We have examined the development of the pattern of functional inputs from the cortex to identified rubrospinal neurons in the cat. To our knowledge, this is the first study concerning the development of functional topography in mammals using synaptic potentials recorded intracellularly in vivo. Our results indicate that the establishment of topography in the corticorubral system starts from a phase of diffuse functional connections before birth, suggesting that cortical axons initially form synapses nonselectively with rubrospinal neurons. The functional topography emerges by the first postnatal week, well before the establishment of an anatomical map, which appears only at approximately P13 by selective axon arborization in topographically appropriate regions (Higashi et al., 1990
EPSP amplitude as an index for studying the development of functional topography
Stimulation of the cortex evoked potentials in rubrospinal neurons in both the fetuses and the neonates. These potentials may or may not be mediated by synapses having the mature type of membrane specializations (Buchanan et al., 1989
At early stages of development, synaptic activity is expected to be subthreshold, as demonstrated in the present study. The corticorubral synaptic activity in the fetal cats would therefore not have been detected with extracellular-recording based techniques. Thus, although technically challenging, it is necessary to record synaptic potentials rather than unit activity to study early development of functional neuronal connectivity.
To use cortically evoked EPSPs to assess the topography of corticorubral connections, it is essential to isolate monosynaptic EPSPs. In principle, the most compelling evidence for a monosynaptic EPSP is that its latency, i.e., the sum of conduction time of the presynaptic axon and a synaptic delay, is less than two synaptic delays. Immature axons, however, have low conduction velocities and thus long conduction times (Song et al., 1995b
EPSP amplitude should reflect the number of functional synapses activated by the cortical stimulation. However, because most of the EPSPs were of complex shape, the total charge transfer might be a better index for estimating the number of input synapses. We thus compared the results using either EPSP amplitude or the integration from the onset to the peak of the EPSPs in 10 randomly selected neurons, but no difference was found. We therefore used EPSP amplitude for all cells for the ease of measurement.
Proliferative versus regressive mechanisms for the formation of topography in the corticorubral connection
Cells showing adult-like functional topography accounted for only approximately half of the cells in the preterm kittens, whereas their proportion increased to >90% over the first postnatal month. These results indicate that functional topography in the corticorubral pathway does not exist at the early stage of cortical innervation but appears to be formed over the period of early postnatal life. The absence of functional topography in the preterm kittens suggests that cortical axons are not strictly guided to topographically correct regions after ingrowth into the RN. This view is consistent with our previous anatomical observations that focally labeled cortical neurons have their axons throughout the RN in preterm cats (Song et al., 1995a
An alternative cellular mechanism for the formation of topography in the corticorubral projection would be that all cortical axons do not enter the RN at the same time, and axons arriving after birth project preferentially to topographically appropriate RN regions. This possibility, however, seems unlikely, because in newborn kittens cortical axons with growing tips were observed in the RN but not along the pathways of the corticorubral projection (our unpublished observation).
Selective formation of synapse as a mechanism for formation of patterned neuronal connectivity
We have shown previously that cortical axons in the RN do not show localized distribution in prenatal cats (Song et al., 1995a
It is surprising that >80% of cells in P1-P8 kittens showed adult-like functional topography, because, anatomically, the corticorubral projection does not exhibit a clear topography until P13 (Higashi et al., 1990
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Figure 8. A schematic summary of the development of functional and anatomical topographic maps in the corticorubral system. The anatomical part is from Higashi et al. (1990)
Although cortical axons arrive at the RN by E50 (Song et al., 1995a
Functional significance
Under the influence of the sensorimotor cortex and the cerebellar deep nuclei, rubrospinal neurons are primarily involved in motor control (Kohlerman et al., 1982
FOOTNOTES Received Jan. 27, 1998; revised July 20, 1998; accepted Aug. 28, 1998.
This work was supported by Grants-in-Aid for Scientific Research on Priority Areas (7279101 and 9280217) and Grants for Young Investigators (9780769) from the Ministry of Education, Science, and Culture of Japan. The authors are investigators of Core Research for Evolutional Science and Technology. We thank Drs. N. Yamamoto and E. S. Ruthazer for discussion and suggestions on this manuscript, M. Kanda for the kittens, and K. Okawa and T. Ohno for help in some of the experiments.
Correspondence should be addressed to Wen-Jie Song, Division of Biophysical Engineering, Graduate School of Engineering Science, Osaka University, Machikaneyama 1-3, Toyonaka 560, Japan.
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