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Addition of fornix transection to frontal-temporal disconnection increases the impairment in object-in-place memory in macaque monkeys.

Wilson CR, Baxter MG, Easton A, Gaffan D - Eur. J. Neurosci. (2008)

Bottom Line: If the contribution of the fornix to scene learning is via interaction with or modulation of frontal-temporal interaction--that is, if they form a unitary system--then Fx should have no further effect when added to frontal-temporal disconnection.However, if the contribution of the fornix is to some extent distinct, then fornix lesions may produce an additional deficit in scene learning beyond that caused by frontal-temporal disconnection.The increased impairment following the addition of Fx provides evidence that the fornix and frontal-inferotemporal interaction make distinct contributions to episodic memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental Psychology, University of Oxford, Oxford, UK. charles.wilson@psy.ox.ac.uk

ABSTRACT
Both frontal-inferotemporal disconnection and fornix transection (Fx) in the monkey impair object-in-place scene learning, a model of human episodic memory. If the contribution of the fornix to scene learning is via interaction with or modulation of frontal-temporal interaction--that is, if they form a unitary system--then Fx should have no further effect when added to frontal-temporal disconnection. However, if the contribution of the fornix is to some extent distinct, then fornix lesions may produce an additional deficit in scene learning beyond that caused by frontal-temporal disconnection. To distinguish between these possibilities, we trained three male rhesus monkeys on the object-in-place scene-learning task. We tested their learning on the task following frontal-temporal disconnection, achieved by crossed unilateral aspiration of the frontal cortex in one hemisphere and the inferotemporal cortex in the other, and again following the addition of Fx. The monkeys were significantly impaired in scene learning following frontal-temporal disconnection, and furthermore showed a significant increase in this impairment following the addition of Fx, from 32.8% error to 40.5% error (chance = 50%). The increased impairment following the addition of Fx provides evidence that the fornix and frontal-inferotemporal interaction make distinct contributions to episodic memory.

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Related in: MedlinePlus

Phase-space plot comparing the current data with those presented in Browning et al. (2005) and Parker & Gaffan (1997b). Data are plotted as mean preoperative percent error against mean postoperative percent error, which allows a comparison of the results of the two studies across a range of preoperative performance, accounting for any possible variation in preoperative performance between the studies. Each point represents the mean pre- vs postoperative performance on a given repetition of lists of new scenes. Therefore, in all four conditions the point representing the first experience of a new set of scenes shows chance performance of approximately 50% in both pre- and postoperative phases, as this is the first time the monkeys see the set of scenes. The dashed diagonal line represents performance that is identical prior to and after surgery. Points below this line represent an improvement from pre- to postoperative performance tests, and points above it represent an impairment in performance from pre- to post-. As learning progresses through the eight repetitions of the scenes, the graph displays the extent to which the improvement with each successive repetition is similar or different pre- and postoperatively. Data for FLxIT are those following the second surgeries in the disconnection procedure, and include two monkeys presented in group FLxIT by Browning et al. (2005). The FLxIT + Fx group represents data following the monkeys' third surgery in the current experiment, and the Bilateral prefrontal cortex (PFC) following their only surgery in Browning et al. (2005). Data from group Fx are those following a second surgery in those monkeys, the first surgery being a sham lesion that had no behavioural effect on this task (see right panel, fig. 1, Parker & Gaffan, 1997b). The FLxIT group shows worse performance than that of group Fx, but both show a postoperative impairment. The FLxIT + Fx group shows similar performance to group Bilateral PFC.
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fig05: Phase-space plot comparing the current data with those presented in Browning et al. (2005) and Parker & Gaffan (1997b). Data are plotted as mean preoperative percent error against mean postoperative percent error, which allows a comparison of the results of the two studies across a range of preoperative performance, accounting for any possible variation in preoperative performance between the studies. Each point represents the mean pre- vs postoperative performance on a given repetition of lists of new scenes. Therefore, in all four conditions the point representing the first experience of a new set of scenes shows chance performance of approximately 50% in both pre- and postoperative phases, as this is the first time the monkeys see the set of scenes. The dashed diagonal line represents performance that is identical prior to and after surgery. Points below this line represent an improvement from pre- to postoperative performance tests, and points above it represent an impairment in performance from pre- to post-. As learning progresses through the eight repetitions of the scenes, the graph displays the extent to which the improvement with each successive repetition is similar or different pre- and postoperatively. Data for FLxIT are those following the second surgeries in the disconnection procedure, and include two monkeys presented in group FLxIT by Browning et al. (2005). The FLxIT + Fx group represents data following the monkeys' third surgery in the current experiment, and the Bilateral prefrontal cortex (PFC) following their only surgery in Browning et al. (2005). Data from group Fx are those following a second surgery in those monkeys, the first surgery being a sham lesion that had no behavioural effect on this task (see right panel, fig. 1, Parker & Gaffan, 1997b). The FLxIT group shows worse performance than that of group Fx, but both show a postoperative impairment. The FLxIT + Fx group shows similar performance to group Bilateral PFC.

Mentions: The comparison of the current results with those from the same task reported previously is informative, and because the testing procedure for the monkeys with FLxIT + Fx is identical to monkeys with bilateral PFC lesions tested by Browning et al. (2005), and monkeys with Fx alone tested by Parker & Gaffan (1997b), a direct comparison of their performance can be made. Figure 5 shows a phase-space plot, in which the postoperative and preoperative learning rates are plotted against each other. The strength of this plot is that it displays the postoperative results of the three studies across a range of preoperative performance levels. This means that a comparison can be made between the studies without concern over any differing levels of preoperative performance between them. Figure 5 shows the effect alone of FLxIT in the current study, in which two animals were the same as those reported in group FLxIT by Browning et al. (2005), and also the effect alone of bilateral Fx in Parker & Gaffan (1997b), in which the monkeys had received a control lesion without behavioural effect on the task prior to Fx. Both of these lesions impair the task, albeit to differing degrees. Figure 5 also shows the increased postoperative impairment following FLxIT + Fx, and demonstrates that at this stage the monkeys' performance was very similar to that of monkeys with bilateral ablation of PFC in Browning et al. (2005). Indeed a one-way anova comparing the performance of the current monkeys at stage FLxIT + Fx and the Group PFC in table 1 of Browning et al. (2005) revealed no significant difference between the two groups, F1,5 = 2.745, P = 0.158.


Addition of fornix transection to frontal-temporal disconnection increases the impairment in object-in-place memory in macaque monkeys.

Wilson CR, Baxter MG, Easton A, Gaffan D - Eur. J. Neurosci. (2008)

Phase-space plot comparing the current data with those presented in Browning et al. (2005) and Parker & Gaffan (1997b). Data are plotted as mean preoperative percent error against mean postoperative percent error, which allows a comparison of the results of the two studies across a range of preoperative performance, accounting for any possible variation in preoperative performance between the studies. Each point represents the mean pre- vs postoperative performance on a given repetition of lists of new scenes. Therefore, in all four conditions the point representing the first experience of a new set of scenes shows chance performance of approximately 50% in both pre- and postoperative phases, as this is the first time the monkeys see the set of scenes. The dashed diagonal line represents performance that is identical prior to and after surgery. Points below this line represent an improvement from pre- to postoperative performance tests, and points above it represent an impairment in performance from pre- to post-. As learning progresses through the eight repetitions of the scenes, the graph displays the extent to which the improvement with each successive repetition is similar or different pre- and postoperatively. Data for FLxIT are those following the second surgeries in the disconnection procedure, and include two monkeys presented in group FLxIT by Browning et al. (2005). The FLxIT + Fx group represents data following the monkeys' third surgery in the current experiment, and the Bilateral prefrontal cortex (PFC) following their only surgery in Browning et al. (2005). Data from group Fx are those following a second surgery in those monkeys, the first surgery being a sham lesion that had no behavioural effect on this task (see right panel, fig. 1, Parker & Gaffan, 1997b). The FLxIT group shows worse performance than that of group Fx, but both show a postoperative impairment. The FLxIT + Fx group shows similar performance to group Bilateral PFC.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2327205&req=5

fig05: Phase-space plot comparing the current data with those presented in Browning et al. (2005) and Parker & Gaffan (1997b). Data are plotted as mean preoperative percent error against mean postoperative percent error, which allows a comparison of the results of the two studies across a range of preoperative performance, accounting for any possible variation in preoperative performance between the studies. Each point represents the mean pre- vs postoperative performance on a given repetition of lists of new scenes. Therefore, in all four conditions the point representing the first experience of a new set of scenes shows chance performance of approximately 50% in both pre- and postoperative phases, as this is the first time the monkeys see the set of scenes. The dashed diagonal line represents performance that is identical prior to and after surgery. Points below this line represent an improvement from pre- to postoperative performance tests, and points above it represent an impairment in performance from pre- to post-. As learning progresses through the eight repetitions of the scenes, the graph displays the extent to which the improvement with each successive repetition is similar or different pre- and postoperatively. Data for FLxIT are those following the second surgeries in the disconnection procedure, and include two monkeys presented in group FLxIT by Browning et al. (2005). The FLxIT + Fx group represents data following the monkeys' third surgery in the current experiment, and the Bilateral prefrontal cortex (PFC) following their only surgery in Browning et al. (2005). Data from group Fx are those following a second surgery in those monkeys, the first surgery being a sham lesion that had no behavioural effect on this task (see right panel, fig. 1, Parker & Gaffan, 1997b). The FLxIT group shows worse performance than that of group Fx, but both show a postoperative impairment. The FLxIT + Fx group shows similar performance to group Bilateral PFC.
Mentions: The comparison of the current results with those from the same task reported previously is informative, and because the testing procedure for the monkeys with FLxIT + Fx is identical to monkeys with bilateral PFC lesions tested by Browning et al. (2005), and monkeys with Fx alone tested by Parker & Gaffan (1997b), a direct comparison of their performance can be made. Figure 5 shows a phase-space plot, in which the postoperative and preoperative learning rates are plotted against each other. The strength of this plot is that it displays the postoperative results of the three studies across a range of preoperative performance levels. This means that a comparison can be made between the studies without concern over any differing levels of preoperative performance between them. Figure 5 shows the effect alone of FLxIT in the current study, in which two animals were the same as those reported in group FLxIT by Browning et al. (2005), and also the effect alone of bilateral Fx in Parker & Gaffan (1997b), in which the monkeys had received a control lesion without behavioural effect on the task prior to Fx. Both of these lesions impair the task, albeit to differing degrees. Figure 5 also shows the increased postoperative impairment following FLxIT + Fx, and demonstrates that at this stage the monkeys' performance was very similar to that of monkeys with bilateral ablation of PFC in Browning et al. (2005). Indeed a one-way anova comparing the performance of the current monkeys at stage FLxIT + Fx and the Group PFC in table 1 of Browning et al. (2005) revealed no significant difference between the two groups, F1,5 = 2.745, P = 0.158.

Bottom Line: If the contribution of the fornix to scene learning is via interaction with or modulation of frontal-temporal interaction--that is, if they form a unitary system--then Fx should have no further effect when added to frontal-temporal disconnection.However, if the contribution of the fornix is to some extent distinct, then fornix lesions may produce an additional deficit in scene learning beyond that caused by frontal-temporal disconnection.The increased impairment following the addition of Fx provides evidence that the fornix and frontal-inferotemporal interaction make distinct contributions to episodic memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental Psychology, University of Oxford, Oxford, UK. charles.wilson@psy.ox.ac.uk

ABSTRACT
Both frontal-inferotemporal disconnection and fornix transection (Fx) in the monkey impair object-in-place scene learning, a model of human episodic memory. If the contribution of the fornix to scene learning is via interaction with or modulation of frontal-temporal interaction--that is, if they form a unitary system--then Fx should have no further effect when added to frontal-temporal disconnection. However, if the contribution of the fornix is to some extent distinct, then fornix lesions may produce an additional deficit in scene learning beyond that caused by frontal-temporal disconnection. To distinguish between these possibilities, we trained three male rhesus monkeys on the object-in-place scene-learning task. We tested their learning on the task following frontal-temporal disconnection, achieved by crossed unilateral aspiration of the frontal cortex in one hemisphere and the inferotemporal cortex in the other, and again following the addition of Fx. The monkeys were significantly impaired in scene learning following frontal-temporal disconnection, and furthermore showed a significant increase in this impairment following the addition of Fx, from 32.8% error to 40.5% error (chance = 50%). The increased impairment following the addition of Fx provides evidence that the fornix and frontal-inferotemporal interaction make distinct contributions to episodic memory.

Show MeSH
Related in: MedlinePlus