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Biological Research

versión impresa ISSN 0716-9760

Biol. Res. v.41 n.4 Santiago dic. 2008

http://dx.doi.org/10.4067/S0716-97602008000400006 

Biol Res 41: 405-412, 2008

The anteromedial extrastriate complex is critical for the use of allocentric visual cues and in the retention of the Lashley III maze task in rats

 

SERGIO ESPINOZA-CIFUENTESa and MARC LEANDER ZEISEa

a Facultad de Humanidades, Escuela de Psicología, Universidad de Santiago de Chile, Santiago, Chile


ABSTRACT

The anteromedial extrastriate complex has been proposed to play an essential role in a spatial orientation system in rats. To gain more information about that possible role, in the present work, two questions were addressed:

1. Are allocentric visual cues relevant for acquisition of the orientation task in the Lashley III maze? 2. Is this integration of allocentric inputs in the anteromedial visual complex relevant in the retention of this test?
While a control group of rats was trained keeping the maze in the same position, the experimental group was trained with the maze rotated counterclockwise by 144 degrees from session to session.
Control rats reached learning criterion significantly earlier and with less errors than the experimental ones (p<.05). After 11 sessions, rats of both groups received stereotaxic injections of ibotenic acid in the anteromedial complex. In the retention test one week after surgery, the control group, which had been able to learn using egocentric and allocentric visual cues, showed a greater déficit than the experimental animáis (p<.05).
These results confirm the role of the anteromedial complex in the processing of visuospatial orientation tasks and demónstrate the integration of allocentric visual cues in the solution of those tasks.

Key terms: visuospatial memory; anteromedial extrastriate complex; Lashley III maze; ibotenic acid; rat.


INTRODUCCION

Studies of the visual system have provided valuable insight into the neural processes underlying our capabilities for navigating in our surroundings and recognizing objects in it. The interdependence of these tasks has been a matter of intense debate (for example “…it is our contention that, despite the protestations of phenomenology, visual perception and the visual control of action depend on functionally and neurally independent systems” (Milner and Goodale, 2006). In this context, it is interesting that the anteromedial and anterior parts of the rat occipital cortex, the AM complex (AMC), a structure formerly considered an area of purely visual reception and recognition because of its retinotopic organization, turned out to be an integrator of diverse input qualities. AMC is one of several retinotopically organized extrastriate visual areas located laterally (in register with Krieg’s area 18a, 1946; or Zilles’s Oc2L, 1985) and medially (Krieg’s area 18; Zilles’s Oc2M) to the primary visual area (striate cortex, area 17, Oc1, V1); Coogan and Burkhalter, 1982; Espinoza and Thomas, 1983; Montero, 1973; Montero, 1981; Montero,1993; Montero et al., 1973a; Olavarría and Montero,1984; Torrealba et al., 1984).

As to the functions of these areas, previous studies have shown that bilateral lesions involving Oc2L reduce visual pattern discrimination (Gallardo et al., 1979; Mc Daniel et al, 1982; Wortwein et al., 1994), while lesions in Oc2M induce
severe déficit in learning a Lashley III maze (Pinto-Hamuy et al., 1975) or a visuosomatic conditioned response (Pinto-Hamuy et al, 1987), in contrast to no learning impediment in rats with lesions in Oc2L. Further studies using ibotenic acid lesions (that leave passing axons intact) restricted to the rostral part of Oc2M, which includes the anteromedial and the anterior extrastriate áreas (anteromedial extrastriate complex, AMC, Montero, 1993) result in visuospatial discrimination déficits (Sánchez et al., 1997) and in a déficit in the acquisition of a visuospatial reference memory task in the Morris water-maze (Espinoza et al., 1999).

Further, it was demonstrated that, when deprived of parts of the AMC, blind rats show seriously reduced performance in their retention capacity tested in the Lashley III maze and that this reduction is tightly correlated to the extensión of the lesión, while no déficit is observed in control rats bearing comparable lesions in VI (Pinto-Hamuy et al., 2004). Thus, the AMC appears to intégrate information from various sensory origins and for learning and retention processes in orientation tasks.

We wondered whether the AMC would also process inputs that are out of reach for the animal and therefore cannot be modified by its behavioral flow (allocentric stimuli as opposed to egocentric ones). Further, we asked whether those stimuli, once integrated in the system would be important to resolve a visual orientation task and whether the intact AMC would be critical for this. To address these questions we designed two experiments:

In the first, we used the Lashley III maze without cover or wire mesh, allowing free visual access to panels and other distant patterns in two groups of rats, impeding the use of those cues in the experimental group by rotating the whole maze after each session while the maze for the control group remained in the same position.

In a second experiment, all rats underwent ibotenic acid lesions that spare axons running through the structure in the AMC to see how their retention of the learned task might be affected.

METHODS

Subjects

Two groups of adult male hooded rats {Rattus norvegicus), of 230 to 310g body weight, were used. The control group (N=9) was trained with the maze always in the same position, while the experimental group (N=9) was trained with the maze rotated 144° counterclockwise (Fig. 1 B) before each session.

Apparatus

The Lashley III maze was used without cover. Otherwise it was the unchanged original (LASHLEY, 1943), with an entrance box, a goal box, eight blind alleys and five decisión points (Fig. 1A). Start and goal boxes were equipped with a sliding door. The apparatus was placed in a room with some panels, drawings and pictures on the walls to provide distal visual cues. Training consisted of one daily session, 5 days a week.

Learning procedure and retention test

To motivate the animáis, they were kept without drinking water during 22 hrs before the training session and rewarded in the goal box with water. They were allowed one trail in the session, counting the errors. It was considered an error when animáis entered with their entire body (except the tail) into a blind alley ("forward error") or made a return to the start box ("backward error"). The learning criterion was no more than one error in two consecutive sessions. After 11 sessions all animáis had reached criterion and underwent lesión surgery.

Seven days after the operation, the retention test was performed. In this session the maze was oriented as in the position for controls (initial orientation for the experimental group).

Surgery

Fifteen minutes after injection of atropine (0.4 mg/kg, i. p.), subjects were anesthetized with sodium pentobarbital (60 mg/kg, i.p.). The scalp was shaved and scrubbed with a 10% iodine solution. After a midline incisión, the posterior neocortex was exposed through trephine holes.

Ibotenic acid (from Sigma; 15 ^g/^1 in saline; pH 7.4; volume 0.5 [xl; speed 0.2 \úl 20 s) was bilaterally injected through a 10 ^il Hamilton syringe at stereotaxic coordinates ML = 3.4 mm and AP = 4.8 mm (interaural line, AP = 0 mm) at a depth of 700 ^im from the cortical surface. These coordinates were derived from previous electrophysiological experiments and cytoarchitectonic data (Espinoza and Thomas, 1983; Montero et al., 1973b; Zules, 1985).

Histology

After the retention test the animáis were sacrificed by an overdose of sodium pentobarbital and perfused through the heart with normal saline followed by 10% formalin buffered solution. Frozen coronal sections were cut at 60 \nm. Every fifth section was mounted and stained with Cresyl violet.

Reconstruction of the lesions

The procedure was the same as used in our previous studies (Sánchez et al, 1997, Espinoza et al, 1999). The sections were examined with a light microscope. The lesioned cortical tissue was identified considering absence of neurons and presence of gliosis. Compromise of white matter was not observed in any of the lesions. The extensión of the lesión was located in drawings enlarged tenfold obtained from optical projections. The drawings were used to produce a dorsal view reconstruction of the lesions by projecting the medial and lateral limit of the lesión on a standard dorsal view of the rat brain. The stereotaxic atlases of Paxinos and Watson (1982) and Zules (1985) were used to estimate the antero-posterior level of the sections. The location of the AMC on this map was estimated on the basis of electrophysiological maps (Espinoza and Thomas, 1983; Montero et al., 1973b). The symmetrically lesioned área was calculated superimposing the compromised área of each hemisphere using a Sigma Sean™ measurement system (Jandel Scientific; Table I and Fig. 3). For practical purposes, the caudal limit of AMC was estimated from AP=4mm, interaural line =0, following the electrophysiological maps already referred to. Some individuáis did not survive the operation and others were detected to have incorrect or insufficient lesions and, consequently, were excluded from evaluation.

Statistics

The Student's í-test was applied comparing the mean error for each group in each session.

In the retention experiment, the mean errors for the two groups were compared using the Mann-Whitney test.

RESULTS

Acquisition

The animáis of the control group, exposed to stable surroundings, reached criterion in 8 sessions or less (average 6.6 ± 1.8 (S.D.)), while the experimental animáis that viewed distant visual stimuli rotated with each session, needed maximallyll (average 9.9 ± 0.9 (S.D.)) sessions (Fig. 2). The difference between these average valúes was significant (independent samples í-test; p = 0.025).

Since conditions were identical for both groups in the first session, errors in this session were not counted. In the remaining 10 sessions, the control group made a total of 117 (average 13.0 ± 7.5 (SD)) and the experimental group 199 (average 22.1 ± 9.0 (SD)) errors. That difference was also significant, although slightly less so than the former one (p = 0.03).

Morphological results

Fig. 3 shows a dorsolateral view of the brains for both groups, the lesions depicted in black. The percentage of bilateral symmetrical lesión of área AMC is indicated for each rat (Fig. 3 and Table I). The solid horizontal line approximates the caudal limit of AMC.

Retention

Retention was tested seven days after surgery for both groups in one session.

The experimental group (N=4) made a total of 2 errors (average = 0.5), the controls (n=4) a total of 19 (average = 4.75). This difference was significant (Mann-Whitney test; p = 0.03).

Most errors in the control group consisted in returning to the start box ("backward errors").

DISCUSSION

The present results show that the AMC is critical for processing allocentic visual inputs in an orientation task. We have shown that distant visual stimuli are in fact used for the orientation task, reducing the number of sessions to reach criterion as well as the number of errors committed during the learning phase. The AMC is critical for that integration because lesions in that área are more compromising for the group of control animáis who could use allocentric cues compared to those who could not.

Recently, Pinto-Hamuy et al., (2004) demonstrated that blind rats, when lesioned in the AMC, have more problems in the retention of the Lashey III maze task than blind controls lesioned in VI, the extensión of the lesión being closely correlated to performance. Taken together with these findings, our data favor the notion that this structure may have the task of integration of information from diverse sensory origins and diverse character participating in orientation, memory storage and retrieval.

These results may also be regarded as a direct corroboration of our previous findings using the Morris Water Maze, showing that similar AMC lesions in the same strain of animáis as used in the present work was critical, producing a severe déficit in the solution of a task in which the animáis had to rely on distal visual cues for navigation (Espinoza et al., 1999).

We suggest that the retinotopy of área AMC is perfectly suited to deal with distal cues, since the receptive fields are considerably larger and with no over-representation of the central visual field as those in VI (Espinoza and Thomas, 1983, Montero et al., 1973b). The present findings are in line with this former result.

In the second part of our experiment, the retention test, the rats of the control group made mainly "backward errors" (they returned to the start box) in contrast to errors in the direction to the goal box ("forward errors"). Backward errors characterized the initial two to three pre-operative learning sessions while the forward errors were more frequent towards the final sessions, so that the control rats with the AMC lesions showed a lack of orientation and behaved as if they were re-learning the maze. The experimental group in contrast made almost no errors. This observation supports the idea mentioned above that the AMC may be considered as part of a system for spatial orientation learning, memory and retrieval.

As to how the AM complex participates in spatial memory mechanisms, there is evidence of a subpopulation of electrophysiologically recorded cells that code mnemonically for directional movement and spatial representations on the basis of visual cues (Chen et al., 1994; McNaughton et al., 1989). Probable neural pathways in rats comprise reciprocal connections of AMC to the retrosplenial cortex (Sanderson et al., 1991;. Torrealba et al.,1984; Vogt and Miller, 1983) and between the retrosplenial cortex and the hippocampal formation (Wyss and VanGroen, 1992) . The hippocampus is implicated in episodic and spatial memory (Rolls, 2000) and contains cells that code for spatial location, the so-called 'place cells' (O'Keefe and Dostrovsky, 1971).

The results show once again the efficacy of restricted ibotenic acid lesión in the induction of a déficit that can be specifically ascribed to neuronal damage in the extrastriate AMC and not to spurious contamination of passing fibers. This method is a valuable tool for analysis of cortical function as was shown with similar lesions in the MT área in monkeys (Pasternak and Merigan, 1994).

Our findings confirm the importance of the rat AMC as crucial for orientation, playing a role in spatial memory mechanisms, and thus can be regarded as homologous to the posterior parietal cortex (PPC) of monkeys (Kolb, 1990, Pinto-Hamuy et al., 2004).

ACKNOWLEDGMENTS

The present work was conducted and supervised by Teresa Pinto-Hamuy who contributed with a first draft for its publication.

This work was supported by project S96081/2, DID, University of Chile to Teresa Pinto and Sergio Espinoza. The authors thank the medical students Pablo Guzman, Rene Jorquera and Solange Ramos for the efficient training of the animáis, the recording of the behavioral data and Dr. Eugenia Díaz for the histological reconstructions. We also owe thanks to Dr. Fernando Torrealba and Dr. Luis Robles for the critical revisión of an early versión of this manuscript.

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Corresponding author: Sergio Espinoza-Cifuentes, sergio.espinoza@usach.cl, Escuela de Psicología, USACH, Av. Ecuador 3650, tercer piso, Phone: (56-2)7184376

Received: March 1, 2008. In Revised form: January 15, 2009. Accepted: January 16, 2009