Forel's Field H Research Articles

Topographic Organization of Excitatory and Inhibitory Commissural Connections in the Superior Colliculi and Their Functional Roles in Saccade Generation

Our electrophysiological study showed that there are topographic connections between excitatory and inhibitory commissural neurons (CNs) in one superior colliculus (SC) and tectoreticular neurons (TRNs) in the opposite SC. To obtain morphological evidence for these topographic commissural connections between the SCs, tracers were injected into various parts of the SC, the inhibitory burst neuron (IBN) area and Forel's field H (FFH), in the cat. Retrogradely labeled CNs were classified into three types according to their somatic areas and identified as GABA-positive or -negative immunohistochemically. Caudal SC injections labeled small GABA-positive CNs (<200 μm(2)) in the deep layers of the opposite rostral SC. Rostral SC injections mainly labeled medium-sized GABA-negative CNs (200-700 μm(2)) in the upper intermediate layer of the opposite rostral SC and small GABA-positive CNs in its deeper layers. Lateral SC injections labeled small GABA-positive CNs in the opposite medial SC and mainly medium-sized GABA-negative CNs in its lateral part. Medial SC injections labeled small GABA-positive CNs in the lateral SC and medium-sized GABA-negative CNs in the medial SC. In comparison, TRNs projecting to the FFH or IBN region were large (>700 μm(2)) and medium-sized. Many of the medium-sized GABA-negative CNs were TRNs projecting to the FFH. These results indicate that mirror-symmetric excitatory pathways link medial to medial (upper field) and lateral to lateral (lower field) parts of the SCs, whereas upper and lower field representations are linked by reciprocal inhibitory pathways in the tectal commissure. These connections presumably play important roles in conjugate upward and downward vertical saccades.

Neural Organization of the Pathways From the Superior Colliculus to Trochlear Motoneurons

The neural organization of the pathways from the superior colliculus (SC) to trochlear motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling techniques. Stimulation of the ipsilateral or contralateral SC evoked excitation and inhibition in trochlear motoneurons with latencies of 1.1-2.3 and 1.1-3.8 ms, respectively, suggesting that the earliest components of excitation and inhibition were disynaptic. A midline section between the two SCs revealed that ipsi- and contralateral SC stimulation evoked disynaptic excitation and inhibition in trochlear motoneurons, respectively. Premotor neurons labeled transneuronally after application of wheat germ agglutinin-conjugated horseradish peroxidase into the trochlear nerve were mainly distributed ipsilaterally in the Forel's field H (FFH) and bilaterally in the interstitial nucleus of Cajal (INC). Consequently, we investigated these two likely intermediaries between the SC and trochlear nucleus electrophysiologically. Stimulation of the FFH evoked ipsilateral mono- and disynaptic excitation and contralateral disynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the ipsilateral SC facilitated FFH-evoked monosynaptic excitation. Stimulation of the INC evoked ipsilateral monosynaptic excitation and inhibition, and contralateral monosynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the contralateral SC facilitated contralateral INC-evoked monosynaptic inhibition. These results revealed a reciprocal input pattern from the SCs to vertical ocular motoneurons in the saccadic system; trochlear motoneurons received disynaptic excitation from the ipsilateral SC via ipsilateral FFH neurons and disynaptic inhibition from the contralateral SC via contralateral INC neurons. These inhibitory INC neurons were considered to be a counterpart of inhibitory burst neurons in the horizontal saccadic system.

Neural Pathways for Vertical Saccades: From the Superior Colliculus to Trochlear Motoneurons

The pathways from the superior colliculus (SC) to vertical ocular motoneurons were analyzed in anesthetized cats using intracellular recording from trochlear motoneurons. Electrical stimulation of the ipsilateral or contralateral SC evoked disynaptic excitation and inhibition in trochlear motoneurons. Stimulation of the ipsilateral Forel's field H (FFH) and the contralateral interstitial nucleus of Cajal (INC) evoked monosynaptic excitation and inhibition in trochlear motoneurons, respectively. Preconditioning stimulation of the SC facilitated FFH-evoked monosynaptic excitation. The results showed that trochlear motoneurons receive disynaptic excitation via the FFH from the ipsilateral SC and disynaptic inhibition via the INC from the contralateral SC.

S-9-1 Clinical values and limitations of SEPs: comparison with depth recording

Projections of neurones in Forel's field H (FFH) to the upper cervical cord and to the lower brainstem were demonstrated by retrograde labelling of the neurones with horseradish peroxidase (HRP). Systematic threshold mapping for evoking antidromic spikes of FFH neurones revealed that they projected to the neck motor nuclei and to pontomedullary reticular formation (PMRF). Stimulation of FFH evoked large monosynaptic excitatory postsynaptic potentials (EPSPs) in reticulospinal neurones (RSNs) of the PMRF, and mono- and disynaptic EPSPs in the dorsal neck motoneurones. Above EPSPs were evoked from areas confined to FFH, thus indicating that they were elicited by stimulation of FFH neurones. Monosynaptic EPSPs in motoneurones were small but disynaptic EPSPs were markedly facilitated following stimulation with train pulses, becoming several times larger than the monosynaptic EPSPs. Disynaptic EPSPs were supposed to be relayed by RSNs in the PMRF which are known to project to dorsal neck motoneurones. The mono- and disynaptic EPSPs were induced chiefly in motoneurones of the head elevator (m. biventer cervicis and complexus) and rarely of the neck lateral flexor (m. splenius). It was suggested that FFH neurones are involved in the control of vertical head movements.

Differential locations in the midbrain of distinct groups of vertical eye movement‐related neurones in cat: their projections and direct connections with oculomotor neurones

The present study was undertaken to investigate the firing patterns, location and projections of vertical eye movement-related neurones in the Forel's field H (FFH), the interstitial nucleus of Cajal (INC), and reticular formation of the mesodiencephalic junction (MDJ) in chronically prepared alert cats. A total of 456 neurones in the medial MDJ with firing closely related to vertical eye movements was examined using antidromic microstimulation and spike-triggered averaging technique. On the basis of their firing patterns, these neurones were classified into five groups, i.e. burst neurones (BNs), burst-tonic neurones (BTNs), tonic neurones (TNs), augmenting neurones (ANs) and pause neurones (PNs). BNs were located mainly in the dorsomedial part of the FFH. Most of TNs were found more caudally than BNs. BTNs and PNs were located further caudally, within the INC and nearby reticular formation. ANs were located mainly in the dorsolateral part of the FFH. Both medium-lead BNs (MLBNs) and BTNs projected to the inferior rectus (IR) subdivision of the oculomotor nucleus on both sides. MLBNs projected to the trochlear nucleus as well through collateral branches of the axon projecting to the oculomotor nucleus. Downward and upward MLBNs made direct excitatory and inhibitory connections, respectively, with IR motorneurones. These results suggest that many kinds of neurones in the paramedian regions of MDJ play a significant role in the genesis of vertical eye movements.

Activity of neurons in Forel's field H during orienting head movements in alert head-free cats.

Single unit activities were recorded in Forel's field H (FFH) at the mesodiencephalic junction during orienting head movements in two alert cats under head-free conditions. Recordings were made of 63 neurons of which 20 showed phasic firing that preceded the onset of head movements by 20-100 ms and was temporally related to the dynamic phase of the orienting head movement. Nineteen of these neurons showed a preference for upward movements, while the remaining neuron preferred downward movements. Activities during orienting movements in eight different directions (each separated by 45 degrees) were systematically analyzed for 12 of the 19 upward-preferring neurons. The activities were broadly tuned; in most of the neurons, maximum activity was observed for direct upward movements (+90 degrees), but significant activity was also observed for ipsilateral and contralateral oblique upward movements (+45 degrees and +135 degrees). In these cases, the increase in activity preceded the onset of the movement. Some increase in activity was also observed for ipsilateral and contralateral horizontal, oblique downward and downward movements. However, the increase in activity in the latter cases occurred simultaneously with or lagged behind the onset of the movement and was often preceded by a decrease in activity. The same pattern of directional tuning was observed in the EMG of the biventer cervicis muscle, a target of FFH neurons. The preferred directions of the 12 upward-preferring neurons were estimated by calculating the vector sum of the activity and were distributed between +68 degrees and +108 degrees. The same amount of activity was observed for ipsilateral and contralateral oblique upward movements, suggesting that FFH neurons on both sides of the brainstem are equally activated even during oblique orienting. Input from the ipsilateral superior colliculus was investigated in 18 neurons, all of which were orthodromically activated with a latency of 0.8-1.8 ms, suggestive of a mono- or disynaptic excitatory connection. Seven neurons were identified as descending projection neurons by antidromic activation from the ipsilateral medullary reticular formation. Repetitive microstimulation of unilateral FFH induced oblique upward head movements and an accompanying torsional component, while simultaneous bilateral stimulation at comparable stimulus strength induced purely upward head movements. These results strongly suggest that the vertical component of orienting head movements is encoded by equal bilateral activation of the FFH.

Axonal trajectories of single Forel's field H neurones in the mesencephalon, pons and medulla oblongata in the cat.

We studied axonal trajectories of single Forel's field H (FFH) neurones (n = 19) in the mesencephalon, pons and medulla by systematic antidromic threshold mapping in cats and differentiated them into two major types. Type I neurones were characterized by projections to the oculomotor nucleus (IIIn) and type II neurones by lack of projections to the IIIn. 2. Type I neurones (11/19) were further classified into three subtypes by the lowest level of projections; type Ic (n = 3) which projected to the cervical cord and type Ib (n = 7) which terminated at the ponto-medullary level and type Ia (n = 1) at more rostral level. In the mesencephalon, stem axons passed just lateral to the IIIn and projected collaterals to the IIIn and the ventral part of the periaqueductal gray matter. In the lower brain stem, stem axons of type Ib and Ic neurones passed in the dorsal part of the reticular formation or in the medial longitudinal fasciculus and projected collaterals to the dorsal part of the nucleus reticularis pontis caudalis (NRPC) and the nucleus reticularis gigantocellularis (NRG) and the reticular formation underlying the nucleus prepositus hypoglossi (PH) and the raphe region. Projections to the superior colliculus were observed in two cases. 3. Type II neurones (8/19) were classified into 2 type IIb projecting to the ponto-medullary reticular formation and 6 type IIc projecting to the cervical spinal cord. In the mesencephalon, stem axons passed through a more lateral region than those of type I and projected collaterals to the mesencephalic reticular formation and the red nucleus. In the lower brain stem, the stem axons passed in the ventral part of the reticular formation corresponding to the central tegmental tract and projected collaterals to the ventral part of the NRPC and NRG. Projections to the interstitial nucleus of Cajal, the inferior olive and the reticular formation underlying the PH were also observed. 4. The dorsal and ventral location of, respectively, stem axons of type I and type II neurones in the lower brain stem was confirmed in a larger number of neurones in experiments with restricted mapping. 5. There was not much difference in location of cell bodies of type I (totally n = 50) and type II (n = 46) neurones. The proportion of spinal-projecting neurones were larger in type II (21/46, 46%) than in type I (7/50, 14%) neurones.

Mono- and disynaptic pathways from Forel's field H to dorsal neck motoneurones in the cat.

1. We analysed the synaptic actions produced by Forel's field H (FFH) neurones on dorsal neck motoneurones and the pathways mediating the effects. 2. Stimulation of ipsilateral FFH induced negative field potentials of several hundred microvolts with the latency of about 1.1 ms in the medial ponto-medullary reticular formation, being largest in the ventral part of the nucleus reticularis pontis caudalis (NRPC), and in the dorsal part of the nucleus reticularis gigantocellularis (NRG). 3. Stimulation of ipsilateral FFH induced excitatory postsynaptic potentials (EPSPs) in 90% (47/52) and inhibitory postsynaptic potentials (IPSPs) in 19% (10/52) of the reticulospinal neurones (RSNs) in the NRPC and the NRG. Latencies of the EPSPs and IPSPs were 0.7-3.0 ms, the majority of which were in the monosynaptic range. The monosynaptic connexions were confirmed by spike triggered averaging technique both in excitatory (n = 4) and inhibitory (n = 2) pathways. 4. Single stimulation of FFH induced EPSPs at the segmental latencies of 0.3-1.0 ms in neck motoneurones, which were clearly in the monosynaptic range. Repetitive stimulation of FFH produced marked temporal facilitation of EPSPs in neck motoneurones. The facilitated components of the EPSPs had a little longer latencies and their amplitude reached several times as large as that evoked by single stimulation in all the tested motoneurones. These facilitated excitations are assumed to be mediated by RSNs in the NRPC and NRG, since RSNs were mono- and polysynaptically fired by stimulation of FFH and they were previously shown to directly project to neck motoneurones. 5. EPSPs were induced in 91% (82/91) of motoneurones supplying m. biventer cervicis and complexus (BCC; head elevator), 10% (3/29) of motoneurones supplying m. splenius (SPL; lateral head flexor). Likewise, stimulation of FFH produced EMG responses in BCC muscles, while not in SPL muscle. Thus FFH neurones produce excitations preferentially in BCC motoneurones. 6. Systematic tracking in and around FFH revealed that the effective sites for evoking above effects were in FFH and extended caudally along their efferent axonal course. 7. These results suggested that FFH neurones connect with neck motoneurones (chiefly BCC, head elevator) mono-, di- and/or polysynaptically and are mainly concerned with the control of vertical head movements.

Activities of forel's field H (FFH) neurones during orienting head movements in alert head-free cats

Activities of forel's field H (FFH) neurones during orienting head movements in alert head-free cats

Cat Pontine Omnipause Neurons: Direct Inhibitory Connection with Forel's Field Burst Neurons Participating in the Genesis of Vertical Saccades

This study investigates synaptic connections of omnipause neurons (OPNs) in the midline pontine tegmentum with vertical medium-lead burst neurons (BNs) in the Forel's field H (FFH), using the microstimulation and spike-triggered averaging techniques in chronically prepared alert cats. OPNs on both sides were antidromically activated by microstimulation at the recording sites of the BNs. Systematic tracking with the stimulating microelectrode revealed indications of profuse axonal branching of OPNs within the BN area. Antidromic spikes of the BNs evoked from the oculomotor nucleus and spike bursts of the BNs associated with saccades were suppressed by OPN area microstimulation. Averaged field potentials in the BN area triggered by spikes of OPNs showed monosynaptic positive waves. These results all but confirm the existence of direct inhibitory synaptic connections of OPNs with the BNs in the FFH. The role of OPNs in the genesis of vertical saccades was also discussed.

Mono- and disynaptic excitatory inputs from the superior colliculus to vertical saccade-related neurons in the cat Forel's field H

Excitatory inputs to neurons in the Forel's field H (FFH) related to visually induced vertical saccades from the ipsilateral superior colliculus (SC) were investigated in chronically prepared alert cats. By stimulation of the deep or intermediate layer of the SC, upward augmenting neurons (ANs) and one long-lead downward burst neuron (BN) were found to be activated monosynaptically, while medium-lead BNs were activated disynaptically. The monosynaptically activated neurons were not antidromically activated from the oculomotor nucleus, whereas disynaptically activated neurons were also activated antidromically from the inferior rectus subdivision of the nucleus. These results suggest that an excitatory input to the FFH from the SC for inducing vertical saccades of visual origin first reaches upward ANs and/or long-lead downward BNs in the FFH, which in turn drive medium-lead BNs in the same area synapsing with motoneurons related to vertical eye movements.

Direct inhibitory synaptic connections of pontine omnipause neurons with burst neurons in Forel's field H related to vertical saccades in the cat

This study investigated synaptic connections of omnipause neurons (OPNs) in the midline pontine tegmentum with medium-lead burst neurons (BNs) in Forel's field H (FFH), using the spike-triggered averaging technique in chronically prepared alert cats. OPNs were identified behaviorally by tonic firing during the intersaccadic period, whereas medium-lead BNs were identified by spike bursts during upward or downward saccades. A positive shift of field potential in the BN area, associated with suppression of the BNs' bursts, was observed during tonic firing of OPNs and during microstimulation in the OPN area. Averaging of BN area field potentials triggered by spikes of single OPNs on both sides, which were antidromically evoked from the BN area, revealed positive waves with monosynaptic latencies. These results strongly suggest that OPNs on both sides make direct inhibitory synaptic connections with vertical eye movement-related medium-lead BNs in the FFH.

Excitatory pathways from Forel's field H to head elevator motoneurones in the cat

Projections of neurones in Forel's field H (FFH) to the upper cervical cord and to the lower brainstem were demonstrated by retrograde labelling of the neurones with horseradish peroxidase (HRP). Systematic threshold mapping for evoking antidromic spikes of FFH neurones revealed that they projected to the neck motor nuclei and to pontomedullary reticular formation (PMRF). Stimulation of FFH evoked large monosynaptic excitatory postsynaptic potentials (EPSPs) in reticulospinal neurones (RSNs) of the PMRF, and mono- and disynaptic EPSPs in the dorsal neck motoneurones. Above EPSPs were evoked from areas confined to FFH, thus indicating that they were elicited by stimulation of FFH neurones. Monosynaptic EPSPs in motoneurones were small but disynaptic EPSPs were markedly facilitated following stimulation with train pulses, becoming several times larger than the monosynaptic EPSPs. Disynaptic EPSPs were supposed to be relayed by RSNs in the PMRF which are known to project to dorsal neck motoneurones. The mono- and disynaptic EPSPs were induced chiefly in motoneurones of the head elevator (m. biventer cervicis and complexus) and rarely of the neck lateral flexor (m. splenius). It was suggested that FFH neurones are involved in the control of vertical head movements.

Subtypes of neurones in Forel's field H as defined by their axonal projection

Projection of neurones in Forel's field H (FFH) to the mesencephalon, the lower brainstem, and the upper cervical spinal cord (C 1) was investigated by threshold mapping for evoking antidromic spikes from these areas. Projections of all FFH neurones tested were ipsilateral. Two main types (Type I and II) and their subtypes were differentiated from the pattern of the trajectories. Type Ia FFH neurones were found to project primarily to the oculomotor nucleus (IIIn) and the periaqueductal gray (PAG) bud did not descend down to the medulla, while Type Ib neurones projected to IIIn, PAG and the nucleus reticularis gigantocellularis (NRG) and Type Ic projected further down to the C 1. Type II neurones were characterized by the absence of collaterals to IIIn. Type IIb projected to the cuneiform, subcuneiform and red nuclei in the mesencephalon and to the NRG, while Type IIc projected further down to the spinal cord. Type IIa neurones which terminated rostral to the NRG were found only rarely. These results suggested that Type Ib and Ic neurones are involved in the control of synergic eye and head movements, while Type IIb, IIc and Ia neurones are specified for the independent control of head and eye movement.

Direct inhibitory projection of pontine omnipause neurons to burst neurons in the Forel's field H controlling vertical eye movement-related motoneurons in the cat.

This study examines the nature of the efferent projection of omnipause neurons (OPNs) in the midline pontine tegmentum to medium-lead burst neurons (BNs) in the Forel's field H (FFH), both of which exhibit activities related to vertical eye movements, using chronically prepared alert cats. Antidromic spikes of the BNs evoked by oculomotor nucleus stimulation were suppressed by shortly preceding (less than 5 ms) microstimulation within the OPN area including actual recording sites of OPNs. Many OPNs were antidromically activated by microstimulation at recording sites of the BNs. Furthermore, systematic tracking in and around the FFH with the stimulating microelectrode substantiated that the OPNs issued axonal branches within the BN area. These results suggest direct inhibitory projection of OPNs to the BNs.

Direct excitatory and inhibitory synaptic inputs from the medial mesodiencephalic junction to motoneurons innervating extraocular oblique muscles in the cat.

This study investigated the nature of synaptic inputs from the Forel's field H (FFH) in the medial mesodiencephalic junction to inferior oblique (IO) motoneurons in the oculomotor nucleus and superior oblique (SO) motoneurons in the trochlear nucleus in anesthetized cats, using intracellular recording techniques. Stimulation of the FFH induced monosynaptic EPSPs in IO motoneurons on both sides. Paired stimulation of the ipsilateral FFH and contralateral vestibular nerve substantiated that the FFH-induced EPSPs were caused mainly by direct excitatory fibers from the FFH to IO motoneurons and partly by axon collaterals of excitatory neurons in the vestibular nuclei. Among parts of the FFH, the medial part was most effective for producing the EPSPs. Systematic tracking with the stimulating electrode in and around the FFH revealed that effective sites of stimulation inducing negative field potentials in the IO subdivision of the oculomotor nucleus, identified as extracellular counterparts of the EPSPs in IO motoneurons, were also located in the interstitial nucleus of Cajal, nearby reticular formation and posterior commissure, besides within and near the medial part of the FFH. Areas far rostral, dorsal and ventral to the FFH were ineffective. EPSP-IPSPs or EPSPs were mainly induced in SO motoneurons on both sides by FFH stimulation. Latencies of these EPSPs and IPSPs were close to those of the EPSPs in IO motoneurons, indicating their monosynaptic nature. Effective stimulation sites for inducing these synaptic potentials overlapped those for the EPSPs in IO motoneurons. Based on these results, it was suggested that excitatory and inhibitory premotor neurons directly controlling IO and SO motoneurons were located within and near the medial part of the FFH.