- Email: [email protected]
Conduction velocity as a parameter in the organisation of the afferent relay in the cat's lateral geniculate nucleus
454
SHOR1 C O M M U N I C A I IONS
Conduction velocity as a parameter in the organisation of the afferent relay in the cat's lateral genlculate nucleus Retinal activity is transmitted most directly to the visual cortex via the lateral geniculate nucleus (LGN) of the thalamus. Two sets of neurones are involved in this transmission, the retinal ganglion cells whose axons form the optic nerve and directly activate the principal or relay cells of the LGN, whose axons project to the visual cortex. Cat optic nerve fibres (i.e., ganglion cell axons) are known to have a wide range of conduction velocities (e.g., refs. 1, 2, 4, 18). We present evidence that LGN cells which are innervated by fast axons from the retina have fast axons projecting to the visual cortex; conversely, cells innervated by slow or intermediate velocity axons have correspondingly slower axons. Experiments were performed on adult cats anaesthetised with nitrous oxide (70 ~ N20/30 ~ OD and paralyzed with gallamine triethiodide (Flaxedil) and toxiferine dichloride. A fuller description of the general experimental organisation is given by Bishop et al. a. A pair of stainless steel electrodes (1 mm bare tips, 4 mm apart) were placed stereotaxically in the optic chiasm (OX), and 6 wire electrodes (1 mm bare tips) were inserted 1-2 mm into area 17 and the 17-18 border of the visual cortex (VC), within the area bounded by the stereotaxic coordinates anterior 0 to --5 mm and lateral 0 to 5 mm. Single L G N cells were recorded with 4 M NaCI filled micropipettes ( < 15 MQ). Only cells activated (by electrical stimulation with 50 /,see pulses of 4-100 V amplitude) both orthodromically from the optic chiasm and antidromically from visual cortex are included in the sample of 84 units in Fig. IF. All were therefore (by definition) relay cells of the LGN. For 76 units we plotted receptive fields as well; all had clearly definable, centre-surround receptive fields of the type described previously for the majority of LGN cells 12Aa. The eyelids were retracted and the pupils dilated with neosynephrine and atropine. Artificial pupils (3 mm in diameter) were used routinely and lenses were used to focus the eyes on the 1 m tangent screen. Receptive fields were plotted with small (0.1-0.2 °) light spots (cJ: ref. 16). Fig. IA-C shows examples of fast, intermediate and slow responding LGN units. In the present sample of 84 units spike latencies to the OX stimulus (measured from the stimulus artefact to the foot of the action spike) ranged from 1.0 to 3.1 msec. Assuming a conduction distance of 20 mm from optic chiasm to LGN, a negligibly small stimulus utilisation time is and a synaptic discharge delay of 0.6-0.8 msec (see below and ref. 19) this range of latencies indicates that the afferent axons varied in velocity from 8 m/sec to 50 m/sec. This range is in good agreement with most earlier reports (e.g. refs. 1, 2, 4, 18). A direct estimate of synaptic discharge delay in the LGN can be made from Fig. 1D, E. A weak electrical stimulus at the optic chiasm evoked only a small presynaptic field potential, labelled pr, and an action spike. This unit had a typical concentric OFF-centre field. Its latency (1.2 msec) is close to the briefest postsynaptic discharge latency observed (Fig. 1F). Reversal of stimulus polarity (lower trace, Fig. 1D, E) allows identification of the artefact. Stimulation at 100/sec caused an increase in spike latency, and in the variability of spike latency (Fig. IE); t h e p r response was
Brain Research, 32 (1971) 454-459
455
SHORT COMMUNICATIONS
A
N=84
"'
2
• •
r=0.805
..w.
•
o
~e
B
• O
z
// /
•
o~°
.'I':'..
.,-.;,
F
w
/
Latency from chiasm(n]s)
1
2
3
C
110
lms --
Latency from
I--
Z
~
2 ~
D
,,-..,.,
3
Latency H ram cortex
U,J
o z
I
w
!
; |
10
l~iil ~iit
s umm e d tenciNes
i
,
i
|
0
2
4
6
LATENCY(ms)
Fig. 1. A, B, C, Responses of 3 LGN units to stimulation of the optic chiasm (OX, left column) and visual cortex (VC, right column). The units in A, B, C are respectively fast, intermediate and slowresponding. The orthodromic (OX) unit responses are superimposed on the LGN field potential, and show some variability in latency. In B and C, extra traces are included to show that, although the responses of intermediate and slow-responding cells were unreliable in occurrence, their spike latency varied over only a small range. Vertical scales indicate 0.5 mV. D, Weak OX stimulation at 1/sec eliciting a small, short latency pre~ynaptic field potential (pr) and postsynaptic spike. Reversal of stimulus polarity (lower trace) allows identification of the artefact. Vertical scale represents 0.5 mV. E, Stimulation at 100/sec caused an increase in the latency and in the latency variation of the spike, confirming that it is postsynaptically activated. The presynaptic potential was unaffected. F, Graph of antidromic latency to VC stimulation against orthodromic latency to OX stimulation for 84 LGN units. The regression lines intersect the abscissa at 0.59 and 0.95 msec. G, Frequency/latency histogram for orthodromic (OX) activation of the 84 LGN units. H, Frequency/latency histogram for antidromic (VC) activation of the 84 LGN units. J, Frequency/latency histogram for summed antidromic and orthodromic latencies of 84 LGN units. Note the contracted abscissa scale relative to F, G and H.
Brain Research, 32 (1971) 454--459
456
SHORt (OMMUNICAI IONS
unaffected. Since the stimulus was near threshold for the whole nerve it is a reasonabIe assumption that some of the fibres generating the presynaptic field (latency (/.6 msec) also elicited (postsynaptically) the spike (latency 1.2 msec at I/sec). The delay of the postsynaptic discharge was thus approximately 0.6 msec for this unit. We consistently found that slow-responding LGN cells could not be reliably activated by every suprathreshold stimulus, although this was always possible for fastresponding cells. This unresponsiveness seemed to be independent of stimulus rate and of stimulus strength (above threshold) and may result from inhibition of the slowresponding LGN cells by interneurones activated by the fast afferents (cf. Fig. 5C in ref. 8). Nevertheless, the latencies of orthodromic spikes evoked in any particular LGN cell, including slow-responding cells, always fell within a narrow range (Fig. 1A-C), about ± 0.1 msec for fast-responding cells, and as much as rE 0.25 msec for the slowest-responding cells. For each cell latency was recorded as the median value of the range. Importantly the latency range in any given cell was always much less than the population range. Moreover, no cell either in the present sample of 84, or among about 100 other LGN cells activated only orthodromically during these experiments, responded with more than one spike. Burst responses were evoked in a number of other cells recorded in and just above the LGN, but none of these cells had the clearcut centre-surround receptive fields typical of LGN cells. None could be activated antidromically from visual cortex, and some responded with a postsynaptic burst discharge to VC stimulation. Cells with similar properties have been considered to be interneuronal in function 7,~°. Thus, individual relay cells of the LGN appear to receive afferents of one predominant conduction velocity and axons with markedly different conduction velocities innervate different LGN cells. Latencies of the antidromic responses of the 84 LGN cells to VC stimulation varied from 0.6 to 2.75 msec. This range is in good agreement with the results of earlier workersS, 21. Latencies as brief as 0.3 msec were reported by Vastola el and were observed in this study for several fibres recorded in the optic radiation above the LGN. Such units were excluded from the present sample. The variability in antidromic latency was much less than for orthodromic activation, and the action spikes often tended to fractionate (Fig. 1A, B; ref. 5). Assuming a conduction distance of 20 mm 21 and negligible stimulus utilisation time, these latencies indicate conduction velocities of 7.2-35 m/sec. Fig. 1F is a plot of antidromic latency against orthodromic latency, for 84 LGN cells. The correlation is statistically significant (r == 0.805, P < 0.001). The two regression lines for the data intercept the abscissa at 0.59 msec and 0.95 msec. As would be expected if the velocity of radiation axons varies linearly with that of tract axons, these intercepts are close to the estimated synaptic delay for the discharge of LGN neurones (see above). Two factors suggest that the latency correlation may be sharper than Fig. l F indicates. First, the results in Fig. IF were pooled from 8 animals, which presumably had slightly different conduction distances and velocities. Second, the histograms in Fig. IG, H which are frequency/latency histograms for the OX and VC stimuli respectively, show only a weak tendency for the units to fall into latency groups, but a clearer picture emerged when the total chiasm-to-cortex latency of each unit was Brain Research, 32 (1971) 454-459
SHORT COMMUNICATIONS
457
considered (Fig. 1J). After adding OX to VC latencies, and hence effectively doubling the conduction distance for each unit, two principal groups appear in our sample. The units forming the fastest group (total latency about 2.0 msec) had latencies to OX stimulation (1.0-1.5 msec) which indicates that they received axons of the fast group described by Bishop et al. 4, which was designated the Fp (fast, peripherally originating) axon group by Stone and Freeman is. The units forming the second peak (total latency about 3 msec) had OX latencies (1.5-1.8 msec) which indicate that they received axons of the slower group of Bishop et al. a, i.e., the Sp (slow peripheral) group of Stone and Freeman. The very slow-activated units (total latency > 3.5 msec) presumably relay the Sc group axons which arise from the area centralis is. Their receptive fields were very small and were close to the presumed fixation point (see below). Two main conclusions can be drawn from these results: (a) each relay cell of the LGN receives its major excitatory retinal input via optic tract axons of one particular conduction velocity, and (b) each relay cell sends to visual cortex an axon whose conduction velocity is directly related to the velocity of its retinal afferents. Noda and Iwama 15 reached essentially the same conclusions for the rat LGN, and Cleland et al. 9 have independently reached these conclusions for the cat. Each LGN relay cell and the retinal afferent or afferents innervating it form a conduction channel which may be characterised by its conduction velocity (i.e., as fast- varying to slow-conducting) and which is, to a considerable degree, separate functionally from channels of different velocity. Three qualifying comments must be made however. First, conduction velocity along any one such channel is not constant. It increases sharply as the optic nerve axons leave the retina (e.g., refs. 1 l, 18) and the scatter in Fig. 1F suggests that there is probably always some change in velocity between optic tract and optic radiation fibres. Nevertheless, velocity relationships are, in general, maintained between retina and cortex. Ganglion cell axons which are relatively fast or slow intraretinally have the same relationship in the optic nerve and tract is and synapse on L G N ceils whose axons are, in general, similarly related (Fig. 1F). Second, the conduction velocity relationships discussed above refer only to the principal excitatory action of retinal afferents on LGN relay cells. Inhibitory or subliminal excitatory effects elicited by retinal afferents of a particular velocity may not be limited to any subgroup of L G N relay cells. Third, despite the relationship evident in Fig. 1F, the total range of retinocortex conduction times between the fastest and the slowest afferents is not great, and its functional significance is not clear (cf. ref. 14). This range can be estimated as follows. The slowest group of optic nerve axons arises from the area centralis and conducts to the optic tract, at a position about 5 mm from the LGN, in 5-6 msec ~s (measured antidromically). Allowing for conduction on to the LGN and for synaptic delay, these axons should evoke discharge in their target LGN cells about 1.0-1.5 msec later. The units in Fig. 1F with correspondingly long orthodromic latencies ( > 2.0 msec) conduct to the visual cortex in 1.5-2.5 msec. Added together these figures suggest a total area centralis-to-visual cortex, conduction time for the slowest fibres of 7.5-10 msec. The comparable conduction time for axons of the fastest group (assuming that they originated at the same distance from the optic disc as the area centralis Brain Research, 32 (1971) 454-459
458
SHOR1 ('OMMUNICAIIONS
(3.2 mmS)) is 4-5 msec. The range o f c o n d u c t i o n times is thus a b o u t 5 msec. This is small when c o m p a r e d , for instance, to the latency o f ganglion cell responses to p h o t i c stimulation, which is in tile o r d e r o f 30-80 msec (e.g., ref. 10). Nevertheless, the o r g a n i s a t i o n o f the L G N relay a c c o r d i n g to c o n d u c t i o n velocity could have c o n s i d e r a b l e functional significance if ganglion cells with different velocity axons have different receptive field properties, since such functional differences w o u l d r e m a i n distinct as far as the visual cortex. T h e r e is, for example, a significant c o r r e l a t i o n in o u r d a t a between latency a n d receptive field diameter, slowerr e s p o n d i n g cells tending to have small fields. T h e smallest fields (0.2-0.75 ° centre d i a m e t e r ) were all found within 4 ° o f the average p o s i t i o n o f a r e a centralis. This is consistent with earlier r e p o r t s that a r e a centralis ganglion cells have very small receptive fields iv, and s l o w - c o n d u c t i n g axons is. M o r e o v e r , Cleland et al. 9 have recently described velocity-related differences in o t h e r receptive field p r o p e r t i e s o f cat retinal ganglion cells. The following p a p e r reports a p r e l i m i n a r y investigation o f the r e l a t i o n s h i p between visual afferent c o n d u c t i o n velocity a n d the receptive field p r o p e r t i e s o f cortical cells. Department of Physiology, The John Curtin School of Medical Research, Australian National University, Canberra (Australia)
JONATHAN STONE KLAUS-PETER HOFFMANN
1 BISHOP,G. H., AND CLARE, M. H., Organization and distribution of fibers in the optic tract of the
cat, J. comp. Neurol., 103 (1955) 269-304. 2 BISHOP, G. H., CLARE,M. H., AND LANDAU,W. M., Further analysis of fibre groups in the optic tract of the cat, Exp. Neurol., 24 (1969) 386-399. 3 BISHOP, P. O., HENRY, G. H., AND SMITH, C. J., Binocular interaction fields in the cat striate cortex, J. Physiol. (Lond.), 216 (1971) 39-68. 4 BISHOP, P. O., JEREMY,D., AND LANCE, J. W., The optic nerve. Properties of a central tract, J. Physiol. (Lond.), 121 (1953) 149-152. 5 BISHOP, P. O., BURKE, W., AND DAVIS, R., Single-unit recording from antidromicallyactivated optic radiation neurones, J. Physiol. (Lond.), 162 (1962) 432-450. 6 BISHOP, P. O., KOZAK, W., AND VAKKUR, G. J., Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co-ordinates and optics, J. Physiol. (Lond.), 163 (1962) 466-502. 7 BURKE,W., AND SEETON, A. J., Discharge patterns of principal cells and interneurones in lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 201-212. 8 BURKE, W., AND SEFTON, A. J., Recovery of responsiveness of cells of lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 213-229. 9 CLELAND, B. G., DUBIN, M. W., ANDLEVlCK,W. R., Sustained and transient neurones in the cat's retina and lateral geniculate nucleus, J. Physiol. (Lond.), (1971) in press. 10 CLELAND, B. G., AND ENROTH-CUGELL, C., Quantitative aspects of gain and latency in the cat retina, J. Physiol. (Lond.), 206 (1970) 73-91. 11 DODT, E., Geschwindigkeit der Nervenleitung innerhalb der Netzhaut, Experientia (Basel), 12 (1956) 34. 12 I-IuBEL, D. H., AND WIESEL, T. N., Integrative action in the cat's lateral geniculate body, J. Physiol. (Lond.), 155 (1961) 385-398. 13 KOZAK,W., RODIECK, R. W., AND BISHOP, P. O., Responses of single units in lateral geniculate nucleus of cat to moving visual patterns, J. Neurophysiol., 28 (1965) 19-47. 14 O~DEN, T. E., AND MILLER, R. F., Studies of the optic nerve of the rhesus monkey: nerve fiber spectrum and physiological properties, Vision Res., 6 0966) 485-506. 15 NODA,H., ANDIWAMA,K., Unitary analysis of retino-geniculate response times in rats, Vision Res., 7 (1967) 205-213. Brain Research, 32 (1971) 454-459
SHORT COMMUNICATIONS
459
16 RODIECK,R. W., AND STONE,J., Analysis of receptive fields of cat retinal ganglion cells, J. Neurophysiol., 28 (1965) 833-849. 17 STONE, J., AND FABIAN, M., Specialized receptive fields in the cat's retina, Science, 152 (1966) 1277-1279. 18 STONE, J., AND FREEMAN, R. B., Conduction velocity groups in the cat's optic nerve classified according to their retinal origin, Exp. Brain Res., (1971) in press. 19 SUMITOMO,I., IDE, K., IWAMA,K., ANDARIKUNI,I., Conduction velocity of optic nerve fibers innervating lateral geniculate body and superior colliculus in the rat, Exp. Neurol., 25 (1969) 378-392. 20 SUZUKI, H., AND KATO, E., Binocular interaction at cat's lateral geniculate body, J. Neurophysiol., 29 (1966) 909-919. 21 VASTOLA,E. F., Conduction velocities in single fibers of the visual radiation, Exp. Neurol., 7 (1963) 1-12. (Accepted June 30th, 1971)
Brain Research, 32 (1971) 454-459
SHOR1 C O M M U N I C A I IONS
Conduction velocity as a parameter in the organisation of the afferent relay in the cat's lateral genlculate nucleus Retinal activity is transmitted most directly to the visual cortex via the lateral geniculate nucleus (LGN) of the thalamus. Two sets of neurones are involved in this transmission, the retinal ganglion cells whose axons form the optic nerve and directly activate the principal or relay cells of the LGN, whose axons project to the visual cortex. Cat optic nerve fibres (i.e., ganglion cell axons) are known to have a wide range of conduction velocities (e.g., refs. 1, 2, 4, 18). We present evidence that LGN cells which are innervated by fast axons from the retina have fast axons projecting to the visual cortex; conversely, cells innervated by slow or intermediate velocity axons have correspondingly slower axons. Experiments were performed on adult cats anaesthetised with nitrous oxide (70 ~ N20/30 ~ OD and paralyzed with gallamine triethiodide (Flaxedil) and toxiferine dichloride. A fuller description of the general experimental organisation is given by Bishop et al. a. A pair of stainless steel electrodes (1 mm bare tips, 4 mm apart) were placed stereotaxically in the optic chiasm (OX), and 6 wire electrodes (1 mm bare tips) were inserted 1-2 mm into area 17 and the 17-18 border of the visual cortex (VC), within the area bounded by the stereotaxic coordinates anterior 0 to --5 mm and lateral 0 to 5 mm. Single L G N cells were recorded with 4 M NaCI filled micropipettes ( < 15 MQ). Only cells activated (by electrical stimulation with 50 /,see pulses of 4-100 V amplitude) both orthodromically from the optic chiasm and antidromically from visual cortex are included in the sample of 84 units in Fig. IF. All were therefore (by definition) relay cells of the LGN. For 76 units we plotted receptive fields as well; all had clearly definable, centre-surround receptive fields of the type described previously for the majority of LGN cells 12Aa. The eyelids were retracted and the pupils dilated with neosynephrine and atropine. Artificial pupils (3 mm in diameter) were used routinely and lenses were used to focus the eyes on the 1 m tangent screen. Receptive fields were plotted with small (0.1-0.2 °) light spots (cJ: ref. 16). Fig. IA-C shows examples of fast, intermediate and slow responding LGN units. In the present sample of 84 units spike latencies to the OX stimulus (measured from the stimulus artefact to the foot of the action spike) ranged from 1.0 to 3.1 msec. Assuming a conduction distance of 20 mm from optic chiasm to LGN, a negligibly small stimulus utilisation time is and a synaptic discharge delay of 0.6-0.8 msec (see below and ref. 19) this range of latencies indicates that the afferent axons varied in velocity from 8 m/sec to 50 m/sec. This range is in good agreement with most earlier reports (e.g. refs. 1, 2, 4, 18). A direct estimate of synaptic discharge delay in the LGN can be made from Fig. 1D, E. A weak electrical stimulus at the optic chiasm evoked only a small presynaptic field potential, labelled pr, and an action spike. This unit had a typical concentric OFF-centre field. Its latency (1.2 msec) is close to the briefest postsynaptic discharge latency observed (Fig. 1F). Reversal of stimulus polarity (lower trace, Fig. 1D, E) allows identification of the artefact. Stimulation at 100/sec caused an increase in spike latency, and in the variability of spike latency (Fig. IE); t h e p r response was
Brain Research, 32 (1971) 454-459
455
SHORT COMMUNICATIONS
A
N=84
"'
2
• •
r=0.805
..w.
•
o
~e
B
• O
z
// /
•
o~°
.'I':'..
.,-.;,
F
w
/
Latency from chiasm(n]s)
1
2
3
C
110
lms --
Latency from
I--
Z
~
2 ~
D
,,-..,.,
3
Latency H ram cortex
U,J
o z
I
w
!
; |
10
l~iil ~iit
s umm e d tenciNes
i
,
i
|
0
2
4
6
LATENCY(ms)
Fig. 1. A, B, C, Responses of 3 LGN units to stimulation of the optic chiasm (OX, left column) and visual cortex (VC, right column). The units in A, B, C are respectively fast, intermediate and slowresponding. The orthodromic (OX) unit responses are superimposed on the LGN field potential, and show some variability in latency. In B and C, extra traces are included to show that, although the responses of intermediate and slow-responding cells were unreliable in occurrence, their spike latency varied over only a small range. Vertical scales indicate 0.5 mV. D, Weak OX stimulation at 1/sec eliciting a small, short latency pre~ynaptic field potential (pr) and postsynaptic spike. Reversal of stimulus polarity (lower trace) allows identification of the artefact. Vertical scale represents 0.5 mV. E, Stimulation at 100/sec caused an increase in the latency and in the latency variation of the spike, confirming that it is postsynaptically activated. The presynaptic potential was unaffected. F, Graph of antidromic latency to VC stimulation against orthodromic latency to OX stimulation for 84 LGN units. The regression lines intersect the abscissa at 0.59 and 0.95 msec. G, Frequency/latency histogram for orthodromic (OX) activation of the 84 LGN units. H, Frequency/latency histogram for antidromic (VC) activation of the 84 LGN units. J, Frequency/latency histogram for summed antidromic and orthodromic latencies of 84 LGN units. Note the contracted abscissa scale relative to F, G and H.
Brain Research, 32 (1971) 454--459
456
SHORt (OMMUNICAI IONS
unaffected. Since the stimulus was near threshold for the whole nerve it is a reasonabIe assumption that some of the fibres generating the presynaptic field (latency (/.6 msec) also elicited (postsynaptically) the spike (latency 1.2 msec at I/sec). The delay of the postsynaptic discharge was thus approximately 0.6 msec for this unit. We consistently found that slow-responding LGN cells could not be reliably activated by every suprathreshold stimulus, although this was always possible for fastresponding cells. This unresponsiveness seemed to be independent of stimulus rate and of stimulus strength (above threshold) and may result from inhibition of the slowresponding LGN cells by interneurones activated by the fast afferents (cf. Fig. 5C in ref. 8). Nevertheless, the latencies of orthodromic spikes evoked in any particular LGN cell, including slow-responding cells, always fell within a narrow range (Fig. 1A-C), about ± 0.1 msec for fast-responding cells, and as much as rE 0.25 msec for the slowest-responding cells. For each cell latency was recorded as the median value of the range. Importantly the latency range in any given cell was always much less than the population range. Moreover, no cell either in the present sample of 84, or among about 100 other LGN cells activated only orthodromically during these experiments, responded with more than one spike. Burst responses were evoked in a number of other cells recorded in and just above the LGN, but none of these cells had the clearcut centre-surround receptive fields typical of LGN cells. None could be activated antidromically from visual cortex, and some responded with a postsynaptic burst discharge to VC stimulation. Cells with similar properties have been considered to be interneuronal in function 7,~°. Thus, individual relay cells of the LGN appear to receive afferents of one predominant conduction velocity and axons with markedly different conduction velocities innervate different LGN cells. Latencies of the antidromic responses of the 84 LGN cells to VC stimulation varied from 0.6 to 2.75 msec. This range is in good agreement with the results of earlier workersS, 21. Latencies as brief as 0.3 msec were reported by Vastola el and were observed in this study for several fibres recorded in the optic radiation above the LGN. Such units were excluded from the present sample. The variability in antidromic latency was much less than for orthodromic activation, and the action spikes often tended to fractionate (Fig. 1A, B; ref. 5). Assuming a conduction distance of 20 mm 21 and negligible stimulus utilisation time, these latencies indicate conduction velocities of 7.2-35 m/sec. Fig. 1F is a plot of antidromic latency against orthodromic latency, for 84 LGN cells. The correlation is statistically significant (r == 0.805, P < 0.001). The two regression lines for the data intercept the abscissa at 0.59 msec and 0.95 msec. As would be expected if the velocity of radiation axons varies linearly with that of tract axons, these intercepts are close to the estimated synaptic delay for the discharge of LGN neurones (see above). Two factors suggest that the latency correlation may be sharper than Fig. l F indicates. First, the results in Fig. IF were pooled from 8 animals, which presumably had slightly different conduction distances and velocities. Second, the histograms in Fig. IG, H which are frequency/latency histograms for the OX and VC stimuli respectively, show only a weak tendency for the units to fall into latency groups, but a clearer picture emerged when the total chiasm-to-cortex latency of each unit was Brain Research, 32 (1971) 454-459
SHORT COMMUNICATIONS
457
considered (Fig. 1J). After adding OX to VC latencies, and hence effectively doubling the conduction distance for each unit, two principal groups appear in our sample. The units forming the fastest group (total latency about 2.0 msec) had latencies to OX stimulation (1.0-1.5 msec) which indicates that they received axons of the fast group described by Bishop et al. 4, which was designated the Fp (fast, peripherally originating) axon group by Stone and Freeman is. The units forming the second peak (total latency about 3 msec) had OX latencies (1.5-1.8 msec) which indicate that they received axons of the slower group of Bishop et al. a, i.e., the Sp (slow peripheral) group of Stone and Freeman. The very slow-activated units (total latency > 3.5 msec) presumably relay the Sc group axons which arise from the area centralis is. Their receptive fields were very small and were close to the presumed fixation point (see below). Two main conclusions can be drawn from these results: (a) each relay cell of the LGN receives its major excitatory retinal input via optic tract axons of one particular conduction velocity, and (b) each relay cell sends to visual cortex an axon whose conduction velocity is directly related to the velocity of its retinal afferents. Noda and Iwama 15 reached essentially the same conclusions for the rat LGN, and Cleland et al. 9 have independently reached these conclusions for the cat. Each LGN relay cell and the retinal afferent or afferents innervating it form a conduction channel which may be characterised by its conduction velocity (i.e., as fast- varying to slow-conducting) and which is, to a considerable degree, separate functionally from channels of different velocity. Three qualifying comments must be made however. First, conduction velocity along any one such channel is not constant. It increases sharply as the optic nerve axons leave the retina (e.g., refs. 1 l, 18) and the scatter in Fig. 1F suggests that there is probably always some change in velocity between optic tract and optic radiation fibres. Nevertheless, velocity relationships are, in general, maintained between retina and cortex. Ganglion cell axons which are relatively fast or slow intraretinally have the same relationship in the optic nerve and tract is and synapse on L G N ceils whose axons are, in general, similarly related (Fig. 1F). Second, the conduction velocity relationships discussed above refer only to the principal excitatory action of retinal afferents on LGN relay cells. Inhibitory or subliminal excitatory effects elicited by retinal afferents of a particular velocity may not be limited to any subgroup of L G N relay cells. Third, despite the relationship evident in Fig. 1F, the total range of retinocortex conduction times between the fastest and the slowest afferents is not great, and its functional significance is not clear (cf. ref. 14). This range can be estimated as follows. The slowest group of optic nerve axons arises from the area centralis and conducts to the optic tract, at a position about 5 mm from the LGN, in 5-6 msec ~s (measured antidromically). Allowing for conduction on to the LGN and for synaptic delay, these axons should evoke discharge in their target LGN cells about 1.0-1.5 msec later. The units in Fig. 1F with correspondingly long orthodromic latencies ( > 2.0 msec) conduct to the visual cortex in 1.5-2.5 msec. Added together these figures suggest a total area centralis-to-visual cortex, conduction time for the slowest fibres of 7.5-10 msec. The comparable conduction time for axons of the fastest group (assuming that they originated at the same distance from the optic disc as the area centralis Brain Research, 32 (1971) 454-459
458
SHOR1 ('OMMUNICAIIONS
(3.2 mmS)) is 4-5 msec. The range o f c o n d u c t i o n times is thus a b o u t 5 msec. This is small when c o m p a r e d , for instance, to the latency o f ganglion cell responses to p h o t i c stimulation, which is in tile o r d e r o f 30-80 msec (e.g., ref. 10). Nevertheless, the o r g a n i s a t i o n o f the L G N relay a c c o r d i n g to c o n d u c t i o n velocity could have c o n s i d e r a b l e functional significance if ganglion cells with different velocity axons have different receptive field properties, since such functional differences w o u l d r e m a i n distinct as far as the visual cortex. T h e r e is, for example, a significant c o r r e l a t i o n in o u r d a t a between latency a n d receptive field diameter, slowerr e s p o n d i n g cells tending to have small fields. T h e smallest fields (0.2-0.75 ° centre d i a m e t e r ) were all found within 4 ° o f the average p o s i t i o n o f a r e a centralis. This is consistent with earlier r e p o r t s that a r e a centralis ganglion cells have very small receptive fields iv, and s l o w - c o n d u c t i n g axons is. M o r e o v e r , Cleland et al. 9 have recently described velocity-related differences in o t h e r receptive field p r o p e r t i e s o f cat retinal ganglion cells. The following p a p e r reports a p r e l i m i n a r y investigation o f the r e l a t i o n s h i p between visual afferent c o n d u c t i o n velocity a n d the receptive field p r o p e r t i e s o f cortical cells. Department of Physiology, The John Curtin School of Medical Research, Australian National University, Canberra (Australia)
JONATHAN STONE KLAUS-PETER HOFFMANN
1 BISHOP,G. H., AND CLARE, M. H., Organization and distribution of fibers in the optic tract of the
cat, J. comp. Neurol., 103 (1955) 269-304. 2 BISHOP, G. H., CLARE,M. H., AND LANDAU,W. M., Further analysis of fibre groups in the optic tract of the cat, Exp. Neurol., 24 (1969) 386-399. 3 BISHOP, P. O., HENRY, G. H., AND SMITH, C. J., Binocular interaction fields in the cat striate cortex, J. Physiol. (Lond.), 216 (1971) 39-68. 4 BISHOP, P. O., JEREMY,D., AND LANCE, J. W., The optic nerve. Properties of a central tract, J. Physiol. (Lond.), 121 (1953) 149-152. 5 BISHOP, P. O., BURKE, W., AND DAVIS, R., Single-unit recording from antidromicallyactivated optic radiation neurones, J. Physiol. (Lond.), 162 (1962) 432-450. 6 BISHOP, P. O., KOZAK, W., AND VAKKUR, G. J., Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co-ordinates and optics, J. Physiol. (Lond.), 163 (1962) 466-502. 7 BURKE,W., AND SEETON, A. J., Discharge patterns of principal cells and interneurones in lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 201-212. 8 BURKE, W., AND SEFTON, A. J., Recovery of responsiveness of cells of lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 213-229. 9 CLELAND, B. G., DUBIN, M. W., ANDLEVlCK,W. R., Sustained and transient neurones in the cat's retina and lateral geniculate nucleus, J. Physiol. (Lond.), (1971) in press. 10 CLELAND, B. G., AND ENROTH-CUGELL, C., Quantitative aspects of gain and latency in the cat retina, J. Physiol. (Lond.), 206 (1970) 73-91. 11 DODT, E., Geschwindigkeit der Nervenleitung innerhalb der Netzhaut, Experientia (Basel), 12 (1956) 34. 12 I-IuBEL, D. H., AND WIESEL, T. N., Integrative action in the cat's lateral geniculate body, J. Physiol. (Lond.), 155 (1961) 385-398. 13 KOZAK,W., RODIECK, R. W., AND BISHOP, P. O., Responses of single units in lateral geniculate nucleus of cat to moving visual patterns, J. Neurophysiol., 28 (1965) 19-47. 14 O~DEN, T. E., AND MILLER, R. F., Studies of the optic nerve of the rhesus monkey: nerve fiber spectrum and physiological properties, Vision Res., 6 0966) 485-506. 15 NODA,H., ANDIWAMA,K., Unitary analysis of retino-geniculate response times in rats, Vision Res., 7 (1967) 205-213. Brain Research, 32 (1971) 454-459
SHORT COMMUNICATIONS
459
16 RODIECK,R. W., AND STONE,J., Analysis of receptive fields of cat retinal ganglion cells, J. Neurophysiol., 28 (1965) 833-849. 17 STONE, J., AND FABIAN, M., Specialized receptive fields in the cat's retina, Science, 152 (1966) 1277-1279. 18 STONE, J., AND FREEMAN, R. B., Conduction velocity groups in the cat's optic nerve classified according to their retinal origin, Exp. Brain Res., (1971) in press. 19 SUMITOMO,I., IDE, K., IWAMA,K., ANDARIKUNI,I., Conduction velocity of optic nerve fibers innervating lateral geniculate body and superior colliculus in the rat, Exp. Neurol., 25 (1969) 378-392. 20 SUZUKI, H., AND KATO, E., Binocular interaction at cat's lateral geniculate body, J. Neurophysiol., 29 (1966) 909-919. 21 VASTOLA,E. F., Conduction velocities in single fibers of the visual radiation, Exp. Neurol., 7 (1963) 1-12. (Accepted June 30th, 1971)
Brain Research, 32 (1971) 454-459