Extrastriate connectivity of the mouse dorsal lateral geniculate thalamic nucleus

The mammalian visual system is one of the most well-studied brain systems. Visual information from the retina is relayed to the dorsal lateral geniculate nucleus of the thalamus (LGd). The LGd then projects topographically to primary visual cortex (VISp) to mediate visual perception. In this view, the VISp is a critical network hub where visual information must traverse LGd–VISp circuits to reach higher order “extrastriate” visual cortices, which surround the VISp on its medial and lateral borders. However, decades of conflicting reports in a variety of mammals support or refute the existence of extrastriate LGd connections that can bypass the VISp. Here, we provide evidence of bidirectional extrastriate connectivity with the mouse LGd. Using small, discrete coinjections of anterograde and retrograde tracers within the thalamus and cortex, our cross-validated approach identified bidirectional connectivity between LGd and extrastriate visual cortices. We find robust reciprocal connectivity of the medial extrastriate regions with LGd neurons distributed along the “ventral strip” border with the intergeniculate leaflet. In contrast, LGd input to lateral extrastriate regions is sparse, but lateral extrastriate regions return stronger descending projections to localized LGd areas. We show further evidence that axons from lateral extrastriate regions can overlap onto medial extrastriate-projecting LGd neurons in the ventral strip, providing a putative subcortical LGd pathway for communication between medial and lateral extrastriate regions. Overall, our findings support the existence of extrastriate LGd circuits and provide novel understanding of LGd organization in rodent visual system.     

Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat

The terminals of axons projecting to the dorsal lateral geniculate nucleus from the thalamic reticular nucleus were identified by electron microscopy 8–24 h after placing small lesions in the ipsilateral reticular nucleus. The terminals contained flattened synaptic vesicles and made Gray type II axo-dendritic synaptic contacts with geniculate neurons. Their identification as F-axons accords well with physiological evidence for a powerful monosynaptic inhibitory input to geniculocortical projection cells from reticular nucleus neurons.     

Ventral lateral geniculate nucleus projects to the dorsal lateral geniculate nucleus in the cat

The lamina C3 of the dorsal lateral geniculate nucleus of the cat does not receive retinal projections but instead receives visual information from the small subpopulation of W-type ganglion cells via the upper substratum of the stratum griseum superficiale of the superior colliculus. We herein report a projection from the lateral division of the ventral lateral geniculate nucleus into the lamina C3 of the dorsal lateral geniculate nucleus. As the lateral division receives projections from the contralateral retina and the ipsilateral upper stratum griseum superficiale of the superior colliculus, we suggest that these regions make up a small cell type W-cell neuronal network that provides visual information to layer I of the striate cortex via the lamina C3.     

Synaptic organization of thalamocortical axon collaterals in the perigeniculate nucleus and dorsal lateral geniculate nucleus

We examined the synaptic targets of large non-gamma-aminobutyric acid (GABA)-ergic profiles that contain round vesicles and dark mitochondria (RLD profiles) in the perigeniculate nucleus (PGN) and the dorsal lateral geniculate nucleus (dLGN). RLD profiles can provisionally be identified as the collaterals of thalamocortical axons, because their ultrastrucure is distinct from all other previously described dLGN inputs. We also found that RLD profiles are larger than cholinergic terminals and contain the type 2 vesicular glutamate transporter. RLD profiles are distributed throughout the PGN and are concentrated within the interlaminar zones (IZs) of the dLGN, regions distinguished by dense binding of Wisteria floribunda agglutinin (WFA). To determine the synaptic targets of thalamocortical axon collaterals, we examined RLD profiles in the PGN and dLGN in tissue stained for GABA. For the PGN, we found that all RLD profiles make synaptic contacts with GABAergic PGN somata, dendrites, and spines. In the dLGN, RLD profiles primarily synapse with GABAergic dendrites that contain vesicles (F2 profiles) and non-GABAergic dendrites in glomerular arrangements that include triads. Occasional synapses on GABAergic somata and proximal dendrites were also observed in the dLGN. These results suggest that correlated dLGN activity may be enhanced via direct synaptic contacts between thalamocortical cells, whereas noncorrelated activity (such as that occurring during binocular rivalry) could be suppressed via thalamocortical collateral input to PGN cells and dLGN interneurons.     

Serotonin-mediated inhibition from dorsal raphe nucleus of neurons in dorsal lateral geniculate and thalamic reticular nuclei

Electrophysiological studies using rats anesthetized with chloral hydrate were performed to determine whether or not serotonin originating in the dorsal raphe nucleus (DR) acts as an inhibitory transmitter or neuromodulator on neurons of the dorsal lateral geniculate nucleus (LGN) and neurons located in the thalamic reticular nucleus (TRN) immediately rostral to the dorsal LGN. In the LGN, conditioning stimuli applied to the DR preceding test stimulus to the optic tract and visual cortex inhibited orthodromic and antidromic spikes in about one-third of the relay neurons and in more than half of the intrageniculate interneurons. Conditioning stimulation of the DR also produced an inhibition of the spikes elicited by stimulation of the optic tract and visual cortex of at least three-quarters of the TRN neurons. Iontophoretic application of serotonin (25 nA) inhibited the orthodromic spikes of the LGN relay neuron and TRN neuron. A close correlation was observed between the effects of DR conditioning stimulation and iontophoretic serotonin in the same neurons. The inhibition with DR conditioning stimulation and iontophoretically applied serotonin was antagonized during iontophoretic application of methysergide (15-40 nA), a serotonin antagonist. These results strongly suggest that serotonin derived from the DR acts on the LGN and TRN neurons as an inhibitory transmitter or neuromodulator to inhibit transmission in these nuclei.     

GABA-immunoreactive neurons in the rat dorsal lateral geniculate nucleus: light microscopical observations

The dorsal lateral geniculate nucleus (dLGN) of the rat was investigated immunocytochemically using an antiserum against the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). The appearance of GABA-immunopositive dendrites, dendritic appendages, and the size and shape of neuronal somata closely resembled the putative intrinsic neurons described previously in Golgi-impregnation studies of the rat dLGN.     

Neurons of the dorsal lateral geniculate nucleus of the albino rat.

Light and electron microscopic observations were made on the dorsal lateral geniculate nucleus (DLGN) of 33 young adult male albino rats. Three variants of the Golgi silver impregnation technique were employed in the light microscopic studies. Neurons were classified into three categories based on location, dendritic pattern, and dendritic appendages. Type 1 and type 3 neurons were distributed throughout the DLGN. Type 2 neurons were located in the superficial zone. Dendritic appendages of type 1 and type 2 neurons indicated these cells may function as geniculo-cortical relay neurons. The type 3 neurons had lobulated dendritic appendages and an axon that terminated withinthe nucleus. Type 3 neurons may represent Golgi-type-II interneurons. Camera lucida drawings, photomicrographs, and electronmicrographs illustrate the characteristics ofthe three cell types. The literature on ultrastructural and neurophysiological findings may substantiate the presence of three neuronal types. Initially, the rat DLGN does not appear as elaborately organized as the nucleus observed in cats and primates; however, there are notable similarities in neuronal morphology and synaptology.     

Noradrenaline-stimulated inositol phospholipid breakdown in rat dorsal lateral geniculate nucleus neurones

Noradrenaline-stimulated inositol phospholipid breakdown in matched vibratome sections through the rat dorsal lateral geniculate nucleus (dLGN). The response was measured as a large accumulation of [3H]inositol labelled inositol monophosphate and was mediated via activation of alpha 1-adrenergic receptors. Accumulation of [3H]inositol phosphates was reduced in kainic acid-lesioned animals, indicating that this response occurred within dLGN neurones and not afferent terminals. The results implicate inositol phospholipid breakdown as part of the mechanism of noradrenergic neurotransmission within the dLGN.     

Abnormal retinotopic organization of the dorsal lateral geniculate nucleus of the tyrosinase-negative albino cat

Visual defects associated with hypopigmentation have been studied extensively in Siamese and albino cats. Previous research on tyrosinase-negative albino cats has shown that (1) approximately 95% of all nasal and temporal retinal fibers cross at the optic chiasm, and (2) ocular dominance columns normally found in cortex are replaced with hemiretinal domains. In this study, we compared the retinotopic organization of the dorsal lateral geniculate nucleus (LGNd) and visual cortex in albino cats. Extracellular recordings were conducted in the LGNd, area 17, and area 18 of six albino cats. Receptive fields (RFs) were plotted for all sites. We find that, as in albino visual cortex, the albino LGNd contains (1) normal cells with RFs in the visual hemifield contralateral to the recording site (RFc), (2) abnormal cells with RFs in the ipsilateral hemifield (RFi), (3) abnormal cells with dual, mirror-symmetric RFs, one in each hemifield (RFd), and (4) abnormal cells with broad RFs that span the vertical meridian (RFb). Our data indicate that lamina A and lamina A1 consist predominantly of normal RFc and abnormal RFi cells, respectively. The C laminae contain a mixture of RFc, RFi, RFd, and RFb cells. The interlaminar zones contained RFd cells, RFb cells, or both. Thus, the albino LGNd is arranged into hemiretinal and not ocular dominance laminae. Finally, the percentage of normal cells is significantly larger in area 17 (84%) and area 18 (70%) than in the LGNd (46%), suggesting a suppression of abnormal activity in albino cat cortex, which could underlie the existing competence of visual function in albinos.     

Serotonergic inhibition of the dorsal lateral geniculate nucleus

Electrophysiological studies were conducted on chloral hydrate-anesthetized rats to determine if the dorsal raphe nucleus (DR) exerts an inhibitory influence upon the dorsal lateral geniculate nucleus (dLGN), and if this inhibition is mediated by the release of serotonin (5-HT). Conditioning stimuli presented to the DR 100-400 ms before an optic tract (OT) shock significantly lowered the amplitude of OT shock-elicited, postsynaptic, field potentials of less than 3 ms latency. Rare, long-latency, field potentials (greater than 5 ms) were diminished in amplitude when preconditioning intervals were less than 15 ms. Six days after intracerebral injection of the 5-HT neurotoxin, 5,7-dihydroxytryptamine (8 micrograms), into the dLGN, significant reductions were observed in 5-HT and 5-hydroxyindole acetic acid in the dLGN. Field potentials recorded on the sixth day in indoleamine-depleted dLGN were significantly less inhibited by DR preconditioning. Intracerebral injections of a control solution neither altered monoamine levels nor the degree of inhibition by DR preconditioning. These data provide further evidence that inhibition of dLGN by DR is mediated by release of 5-HT.     

Activity-evoked extracellular pH shifts in slices of rat dorsal lateral geniculate nucleus

Activity-dependent extracellular pH shifts were studied in slices of the rat dorsal lateral geniculate nucleus (dLGN) using double-barreled pH-sensitive microelectrodes. In 26 mM HCO₃⁻-buffered media, afferent activation (10 Hz, 5 s) elicited an early alkaline shift of 0.04±0.02 pH units associated with a later, slow acid shift of 0.05±0.03 pH units. Extracellular pH shifts in the ventral lateral geniculate nucleus were rare, and limited to acidifications of approximately 0.02 pH units. The alkaline shift in the dLGN increased in the presence of benzolamide (1–2 μM), an extracellular carbonic anhydrase inhibitor. The mean alkaline shift in benzolamide was 0.10±0.05 pH units. In 26 mM HEPES-buffered saline, the alkaline response averaged 0.09±0.03 pH units. The alkaline shifts persisted in 100 μM picrotoxin (PiTX) but were blocked by 25 μM CNQX/50 μM APV. If stimulation intensity was raised in the presence of CNQX/APV, a second alkalinization arose, presumably due to direct activation of dLGN neurons. The direct responses were amplified by benzolamide, and blocked by either 0 Ca²⁺/EGTA, Cd²⁺ or TTX. In 0 Ca²⁺, addition of 500 μM–5 mM Ba²⁺ restored the alkalosis. Alkaline shifts evoked with extracellular Ba²⁺ were larger and faster than those elicited by equimolar Ca²⁺. In summary, synchronous activation in the dLGN results in an extracellular H⁺ sink, via a Ca²⁺-dependent mechanism, similar to activity-dependent alkaline shifts in hippocampus.     

Response properties of cells in the dorsal lateral geniculate nucleus of the albino rat

The response patterns of cells in the dorsal lateral geniculate nucleus of the albino rat were studied in order to examine the functional organization of the lateral geniculate nucleus. Both photic stimulation and electrical stimulation of the optic tract were used to activate single units in the lateral geniculate nuclei. Three different types of response patterns were found for principal cells, while interneurons all had similar response patterns. The first class of principal cells, E-S cells, responded to stimulation with a period of excitation, followed by a period when activity was suppressed. A second class of cells, S cells, responded to photic stimulation with an initial period when activity was suppressed. The final class of cells, E cells, responded with a period of excitation followed by a return to spontaneous rates of firing. The response patterns of E cells suggest that this type of principal neuron does not receive feedback inhibition of the type proposed in previous models of the lateral geniculate nuclei. Based on these and other observations, a new model of the functional organization of the lateral geniculate nuclei is proposed.     

Retinotopic organization in the dorsal lateral geniculate nucleus of the tammar wallaby (Macropus eugenii)

Electrophysiological recordings were made from 187 single cells in the tammar wallaby (Macropus eugenii) dorsal lateral geniculate nucleus (LGNd). The results show that it is topographically organized such that the superior visual field is represented dorsally, the inferior field is represented ventrally, the nasal visual field is represented caudally, and the temporal visual field is represented rostrally. The visual field of one eye ranges from -30 degrees nasal to +179 degrees temporal in azimuth and +73 degrees superior to -49 degrees inferior in elevation. Ganglion cells that had receptive field positions between -9 degrees and +179 degrees projected to the contralateral LGNd while the ganglion cells that projected to the ipsilateral LGNd had visual fields from 0 to +30 degrees. The binocular visual field extends 60 degrees in azimuth. This representation in the LGNd is expanded relative to the monocular representation. There is also an increased representation of the horizon in the temporal field corresponding to the visual streak of retinal ganglion cells. The binocular visual field is located where contralateral and ipsilateral laminae are shown to interdigitate by proline autoradiography. There are nine eye-specific laminae in the LGNd. Four receive afferents from the contralateral eye and five receive afferents from the ipsilateral eye. The lines of isoelevation are perpendicular to the coronal plane of section while the lines of isoazimuth are nearly parallel to the coronal plane. The lines of projection representing one visual direction are inferred to be perpendicular to the tangent of curvature of the laminae as in the LGNd of other mammals. The majority of cells (85%) recorded had on- or off-centre responses. On- and off-centre responses were not apparently segregated in the LGNd but segregation may not have been revealed by the single-unit recording technique.     

Synaptic development of the mouse dorsal lateral geniculate nucleus

The dorsal lateral geniculate nucleus (dLGN) of the mouse has emerged as a model system in the study of thalamic circuit development. However, there is still a lack of information regarding how and when various types of retinal and nonretinal synapses develop. We examined the synaptic organization of the developing mouse dLGN in the common pigmented C57/BL6 strain, by recording the synaptic responses evoked by electrical stimulation of optic tract axons, and by investigating the ultrastructure of identified synapses. At early postnatal ages (<P12), optic tract evoked responses were primarily excitatory. The full complement of inhibitory responses did not emerge until after eye opening (>P14), when optic tract stimulation routinely evoked an excitatory postsynaptic potential/inhibitory postsynaptic potential (EPSP/IPSP) sequence, with the latter having both a GABA_A and GABA_B component. Electrophysiological and ultrastructural observations were consistent. At P7, many synapses were present, but synaptic profiles lacked the ultrastructural features characteristic of the adult dLGN, and little γ‐aminobutyric acid (GABA) could be detected by using immunocytochemical techniques. In contrast, by P14, GABA staining was robust, mature synaptic profiles of retinal and nonretinal origin were easily distinguished, and the size and proportion of synaptic contacts were similar to those of the adult. The emergence of nonretinal synapses coincides with pruning of retinogeniculate connections, and the transition of retinal activity from spontaneous to visually driven. These results indicate that the synaptic architecture of the mouse dLGN is similar to that of other higher mammals, and thus provides further support for its use as a model system for visual system development. J. Comp. Neurol. 518:622–635, 2010. © 2009 Wiley‐Liss, Inc.     

Postnatal development of the noradrenergic system in the dorsal lateral geniculate nucleus of the rat

The noradrenergic innervation of the developing dorsal lateral geniculate nucleus of the rat was examined with light and electron microscopic immunocytochemistry. At birth, few, relatively thick, noradrenergic fibers innervated the nucleus. Their density was steadily increased and they became thinner, tortuous, and varicose with the progression of age. Only a minority (11-15%) of labeled varicosities made synaptic contacts. Most of these synapses were symmetrical and on dendritic shafts. The present findings demonstrate the establishment of the anatomical relationships between noradrenergic afferents and neurons of the dorsal lateral geniculate nucleus during development and may help to understand the role of noradrenaline in the processing of visual information.     

Complex convolutions in neurons of the dorsal lateral geniculate nucleus of the normal albino rat

The postnatal development of complex convolutions (CCs) of the dorsal lateral geniculate nucleus (LGNd) in normal rats has been studied quantitatively with light microscopy. We report that immature neurons do not contain these scarcely understood organelles, since they can be seen for the first time in very few, mature neurons of the 30 day rat; their number constantly increases during the following 4 months. These cytoplasmic inclusions can be equally seen in the aged rat. CCs are present in neurons of all sizes, except the smallest, which correspond to the interneuron population. Although, morphologically, CCs of the LGNd of the rat are similar, but not identical, to the cytoplasmic multilaminated bodies of the cat, intermediate forms are described.