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. 2010 Feb;17(2):104–108. doi: 10.1101/lm.1647710

Recognition memory: Adding a response deadline eliminates recollection but spares familiarity

Magdalena M Sauvage 1, Zachery Beer 1, Howard Eichenbaum 1,1
PMCID: PMC2825697  PMID: 20154356

Abstract

A current controversy in memory research concerns whether recognition is supported by distinct processes of familiarity and recollection, or instead by a single process wherein familiarity and recollection reflect weak and strong memories, respectively. Recent studies using receiver operating characteristic (ROC) analyses in an animal model have shown that manipulations of the memory demands can eliminate the contribution of familiarity while sparing recollection. Here it is shown that a different manipulation, specifically the addition of a response deadline in recognition testing, results in the opposite performance pattern, eliminating the contribution of recollection while sparing that of familiarity. This dissociation, combined with the earlier findings, demonstrates that familiarity and recollection are differentially sensitive to specific memory demands, strongly supporting the dual process view.

Receiver operating characteristic (ROC) analysis holds the promise of dissecting the contributions to recognition memory of episodic recollection and familiarity (Yonelinas 2001), and this method can be applied equally well to examine these memory processes in animals as well as humans (Fortin et al. 2004; Sauvage et al. 2008). According to the dual process model, recollection is indexed by the asymmetry of the ROC function whereas familiarity is measured by the degree of curvilinearity of that function, and correspondingly, these two parameters can vary independently (Yonelinas 2001). However, there is controversy about this interpretation of ROC components. Some have argued that the asymmetry and curvilinearity of the ROC function both reflect the strength of memories mediated by a single process (Wixted 2007), and correspondingly, these components of the ROC increase or decrease together in stronger or weaker memories, respectively (Squire et al. 2007).

A resolution of this controversy can be advanced by examining whether the ROC asymmetry and curvilinearity are independently influenced by task manipulations that favor either recollection or familiarity, consistent with dual process theory, or instead are similarly influenced by conditions that affect memory strength. Recent data from an animal model of recognition have shown that adding a demand for remembering associations between independent stimuli eliminates the ROC curvilinearity without affecting the asymmetry, consistent with the dual process view (Sauvage et al. 2008; for discussion of associative recognition, see Mayes et al. 2007). However, in order to provide compelling evidence of independence of the two ROC components, it is also critical to show that other memory demands that favor familiarity produce the opposite pattern, elimination of the ROC asymmetry while sparing its curvilinearity. Together these findings would constitute a double dissociation between the two parameters of the ROC function that cannot be explained by a single process theory.

As originally conceived in models proposed in the 1970s, familiarity is characterized as a perceptually driven, pattern matching process that is completed rapidly, whereas recollection is characterized as a conceptually driven, organizational process that requires more time (Mandler 1972; Atkinson and Juola 1973, 1974; for reviews, see Yonelinas 2002; Mandler 2008). Consistent with this view, the results of several studies that employ response deadlines in the test phase report that familiarity is more rapid than recollection. For example, forcing people to make speeded recognition responses has little effect on simple yes–no recognition but strikingly reduces performance when subjects must remember where or when an item was studied (Yonelinas and Jacoby 1994; Gronlund et al. 1997; Hintzman et al. 1998). Other studies that require subjects to oppose familiarity and recollection reveal a two-component temporal function that includes a rapidly available familiarity process and a slower recollective process (Dosher 1984; Gronlund and Ratcliff 1989; Hintzman and Curran 1994; McElree et al. 1999). In addition, studies that measure brain evoked response potentials (ERPs) have revealed two distinct ERP modulations commonly observed during recognition: a mid-frontal negativity onsetting about 400 msec after stimulus onset that is associated with familiarity, and a parietally distributed positivity beginning about 500 msec after stimulus onset that is associated with recollection (Smith 1993; Duzel et al. 1997; Curran 2004; Duarte et al. 2006; Woodruff et al. 2006; but see Voss and Paller 2009).

Dual process theory predicts that applying an appropriate early response deadline should allow sufficient time for contribution of familiarity but not that of recollection, and so should reduce the ROC asymmetry while sparing its curvilinearity, opposite to the already observed effects of associative memory demands that favor recollection (Sauvage et al. 2008). Confirmation of this prediction combined with the previous findings of the opposite effects in associative recognition would constitute a double dissociation between the features of recollection and familiarity. This result would therefore strongly support the conclusion that the asymmetry and curvilinearity are independent parameters of the ROC function that are differentially linked to features of recollection and familiarity, respectively.

Results

We first characterized the ROC functions for recognition memory performance by rats when there was no limit on the time allowed to elicit recognition judgments (no-deadline condition) versus a condition where rats were challenged to respond rapidly (deadline condition). Briefly, during the study phase, rats were presented with a session-unique list of 10 household scents, each mixed with sand in plastic cups. After a 30-min retention delay, memory was tested using a list that included the same 10 odor stimuli (old) intermixed with 10 new odors (Fig. 1A). Following a nonmatching to sample rule, if the test odor was new, the rat could dig in the test cup to retrieve a buried reward; if the stimulus was old, the rat could obtain a reward by refraining from digging in the test cup and instead approach a separate cup at the back of the cage (Fig. 1B). ROC functions were generated by plotting the probability of “hits” (correct recognition of old odors) against the probability of “false alarms” (incorrect recognition of new odors) across five levels of bias toward eliciting old versus new responses. The five bias levels were generated by varying the difficulty and the reward payoff ratio for responding to the test stimulus (Fig. 1C). The best fitting ROC curve was determined using a least-squares model with the recollection (R) and familiarity (d′) as parameters (see Materials and Methods) (Yonelinas et al. 1998). Typically, the ROC function for item recognition is asymmetrical, as reflected by the slope of the z-transformed ROC inferior to 1 and a positive Y-intercept, which is suggested to reflect recollection (Yonelinas 1997; Yonelinas and Parks 2007). In addition, the function is curvilinear in ROC space, while linear in the z-transformed ROC space, which is viewed as reflecting the contribution of familiarity (Yonelinas 1997; Yonelinas and Parks 2007).

Figure 1.

Figure 1.

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Odor recognition task. (A) Odor recognition protocol with examples of odors used during the study and recognition phases of the task. Note the modification in this version of the task over the version reported previously (Fortin et al. 2004) was that the test cup was covered by a lid (shown in gray) after either digging or turning away in the no-deadline condition or at the deadline. (B) Delay nonmatching to sample rule. If the odor was “new,” the rat could dig in the stimulus cup to retrieve a buried reward. If the odor was “old,” the rat had to refrain digging and go to the back of the cage where a reward was dropped. (C) The bias levels obtained by varying the depth of the test cup and the reward payoff ratios. All procedures were approved by the Boston University Institutional Animal Use Committee.

Rats initially performed the task without a response deadline, and response latencies were measured, for each rat at each bias level, as the time between arrival at the target stimulus cup and the initiation of digging (for a “new” odor) or turning away (for an “old” odor). Subsequently, the tests were repeated under identical procedures, except that a response deadline was imposed such that the time allocated to respond was reduced to half of the no-deadline latency for that bias by covering the cup at the deadline time. Under the no-deadline condition, the typical item recognition ROC curve was observed (Fig. 2A), and the shape of the ROC function was studied using model-dependent (R and d′) parameter estimates and model-independent analyses of curve fits (regressions). The ROC function was curvilinear, indicating the contribution of familiarity, as reflected by an index of familiarity (d′) significantly different from 0 (d′ = 0.61, t(4) = 10.65, P < 0.001) (Fig. 2C) and confirmed by a linear z-transformed ROC function (quadratic term of the polynomial regressions on z-ROC functions not different from zero, Fquad: t(4) = 2.41, P > 0.050) (Fig. 2A, inset). In further agreement with the literature, the ROC function was also asymmetrical, indicating that recollection also contributes to recognition performance, as reflected by the slope of the z-transformed linear approximation inferior to 1 (z-ROC slope = 0.78, t(4) = −4.69, P = 0.009; see Materials and Methods) and a positive Y-intercept (R = 0.28, t(4) = 16.19, P < 0.001) (Fig. 2A).

Figure 2.

Figure 2.

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ROC curves and recollection and familiarity indices for odor recognition memory. (A) Under the no-deadline condition, recognition performance was based on a combination of recollection and familiarity as reflected by an asymmetrical and curvilinear ROC function in normal space and confirmed by a linear z-transformed ROC function. (B) In the deadline condition, recollection was selectively reduced, as shown by a decrease of the Y-intercept, whereas familiarity was spared as reflected by a curvilinear and symmetrical ROC function, and confirmed by a linear z-ROC function. (C) Adding a response deadline significantly reduced the recollection index (R) without affecting the familiarity estimate (d′). Values, ± SEM.

In the deadline condition, the response latency was reduced by approximately half for each bias level (Fig. 3). Performance was supported by familiarity as reflected by a curvilinear ROC function (d′ = 0.71 different from 0, t(4) = 10.59, P < 0.001) and a linear z-ROC function with a quadratic coefficient not different from 0 (Fquad: t(4) = 2.28; P > 0.050). However, in striking contrast to the ROC function in the no-deadline condition, recollection did not contribute significantly to recognition performance. The Y-intercept of the ROC curve was reduced to a level not differing from zero (R = 0.06, t(4) = 2.09, P = 0.105) (Fig. 2B,C), and the ROC function became symmetrical, measured as a z-ROC slope not significantly different from 1 (z-ROC slope = 0.98, t(4) = −0.34, P = 0.752). Furthermore, a direct between-group comparison of d′ and R scores with and without the deadline (see Materials and Methods) revealed that adding a deadline affected recollection and familiarity in a differential manner, by reducing the recollection index while sparing the familiarity index (interaction F(1,4) = 56.481, P = 0.002; post-hoc R, t(4) = −6.43, P = 0.003; d′, t(4) = −1.35, P = 0.248) (Fig. 2C). Collectively, these findings support the view that recollection-based responses were relatively slow, and eliminated by the response deadline, whereas familiarity-based responses were accomplished rapidly, within the deadline, consistent with the dual process model.

Figure 3.

Figure 3.

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Response latency at each bias was significantly lower under the deadline condition. Values, ± SEM.

Further analysis revealed that the decrease in the recollection index could be attributed to a reduction of memory for old items and not from an alteration in response bias or false memories, as indicated by a selective decrease in the proportion of hits and no change in false alarms at the most accurate bias level (bias 5: Hitno-deadline = 0.44, Hitdeadline = 0.31, t(4) = −7.84, P = 0.002; Fano-deadline = 0.10, Fadeadline = 0.12, t(4) = 0.96, P = 0.394).

We also retested rats in the no-deadline condition in order to verify that the reduction in recollection observed under the response deadline condition was not due to overtraining. We found that neither the recollection index nor the familiarity index measured for no-deadline retesting significantly differed from those observed under the original no-deadline condition (Roriginal no-deadline = 0.28, Rno-deadline re-testing = 0.33; t(3)− = −2.82, P = 0.067; d′original no-deadline = 0.61, d′no-deadline re-testing = 0.71; t(3) = −1.03, P = 0.381). Moreover, the recollection index under deadline condition was significantly reduced compared with that for the repeated no-deadline condition, while d′ remained unaffected, as was the case compared with the original no-deadline condition (Rdeadline = 0.08, Rno-deadline re-testing = 0.33; t(3) = −6.39, P = 0.008; d′deadline = 0.76, d′no-deadline re-testing = 0.76; t(3) = −0.06, P = 0.958).

Finally, we found that the unequal variance single process model, which assumes different variances for the old and new item distribution (Vold > Vnew = 1), could not account for the performance of rats with speeded responses, because the variance of the old item distribution became equal to that of the new items under response deadline condition (Vold = 1.05, Vnew = 1, t(4) = 0.73, P = 0.503).

Discussion

These data show for the first time that recognition performance can be driven solely by familiarity as defined by the ROC function in normal human or animal subjects. The selective reliance on familiarity observed here complements the opposite finding; that is, selective reliance on recollection when the memory retention interval is elongated (Fortin et al. 2004) and when the task requires memory for associations in the same behavioral paradigm for rats (Sauvage et al. 2008) and in a similar paradigm for humans (Yonelinas 1997). This combination of findings constitutes a double dissociation between the features of recollection and familiarity in rats. Furthermore, these observations show that recollection and familiarity can be manipulated independently and, hence, strongly suggest the existence of two distinct underlying memory processes.

Although speeding responses significantly reduced the contribution of the recollection process to odor recognition memory (P = 0.003), the reduction in the recollection index R was slightly less than that in aged rats or in rats with hippocampal damage performing on the same task (Ryoung − Rold = 0.27 > Rsham − Rhippocampus = 0.23 > Rno deadline − Rdeadline = 0.20) (Fortin et al. 2004; Robitsek et al. 2008). The smaller number of subjects used in the present study could account, at least in part, for this result. Alternatively, the degree of hippocampal dysfunction in aging and restricted damage to the hippocampus in young rats could more dramatically affect the recollection process than a reduction of response latency in intact rats. Also, our designation of the response deadline as half the time of the unrestricted response latency of each rat (see Materials and Methods) is arbitrary and may not have completely eliminated the contribution of recollection.

The conclusion that recollection and familiarity ROC indices are independent is also supported by observations of differential or opposite effects of selective brain damage on recollection and familiarity indices in rats and humans. Studies on humans have reported selective deficits in recollection, sparing familiarity, following hippocampal damage (Yonelinas 2002; Mayes et al. 2004; Aggleton et al. 2005; Vann et al. 2009; but see Wais et al. 2006) and the opposite pattern, impaired familiarity and preserved recollection, following damage to the perirhinal cortex (Bowles et al. 2007). In addition, functional imaging studies have reported double dissociations between brain areas activated in association with recollection- or familiarity-driven memory (e.g., Ranganath et al. 2004; Yonelinas et al. 2005, 2007; Daselaar et al. 2006; Montaldi et al. 2006; but see Shrager et al. 2008; for review, see Eichenbaum et al. 2007). Also, the ROC index of recollection for the recognition of single items was eliminated, while the familiarity was enhanced in aged rat animals that performed exceptionally in overall accuracy (Robitsek et al. 2008). Furthermore, in associative recognition, hippocampal damage reduced the ROC index of recollection but enhanced that of familiarity (Sauvage et al. 2008), consistent with the findings that hippocampal damage results in the unitization of stimulus features, allowing familiarity to support recognition of each unitized stimulus configuration (Quamme et al. 2007).

Combined with the present findings, these studies provide compelling evidence that familiarity and recollection are distinct processes that are differentially sensitive to cognitive variables and compromised brain function.

Materials and Methods

Animals

Male rats (n = 5) were maintained under reverse light/dark cycle (06:00 h light off, 18:00 h light on) and tested during the day.

Behavioral protocol

The behavioral paradigm is similar to the design published earlier (Fortin et al. 2004). During shaping, rats learned to retrieve one-fourth of a piece of Froot Loop (Kellogg's) cereal buried in a 125-mL plastic cup (NALGENE) filled with unscented sand. Then, animals were trained on a delayed nonmatching to sample task. To ensure the task could not be solved by smelling the reward buried under the sand, all cups were baited but the reward was not accessible to the animal for the “old” odors. During initial trials, in the study phase one stimulus composed of an odor mixed with sand and baited with 1/4 Froot Loop was presented; after a 1-min delay, the same odor (old) and a new odor were presented successively in a pseudorandom order. After the rat either dug or turned away from the test cup, the cup was covered. As animals learned (80% correct over three consecutive 10 trial sessions), the number of odors presented during the study phase increased gradually from one to 10 and, correspondingly, that for the test phase increased from two to 20, and the delay between study and test phase increased gradually from 1 min to 30 min. Once rats reached criterion performance, they were overtrained for 10 additional sessions. Training lasted approximately 2 mo. Subsequently, a set of five different bias levels that involved different combinations of cup sizes and amount of reward was introduced (bias levels, 1–5). Each bias level was used in one of five sessions per week in a pseudorandom order. Once P(Hit) and P(Fa) were within a range of 0.2 for each bias, data were collected for four additional sessions at each bias and averaged to plot individual no-deadline ROC curves and generate R and d′ values. Performance was videotaped to score response latencies for each rat at each bias level. In the subsequent deadline condition testing, the time allocated for the rat to respond was reduced to half of the average latency at each bias level scored for each rat by covering the test cup at the deadline. Once rats were habituated to the deadline procedure (five sessions total, one for each bias), data were collected for four additional sessions at each bias and averaged to generate individual deadline ROC curves and calculate R and d′ indices. To control for the possibility of an effect of overtraining on the recollection and familiarity indices under deadline condition, testing was repeated under the no-deadline condition. Once rats were habituated to the no-deadline procedure again (five sessions total, one for each bias), data were collected for two additional sessions at each bias, and R and d′ indices were calculated. One rat stopped responding after the deadline condition and, hence, did not contribute to the no-deadline retesting analysis. Paired t-tests were used for all statistical analysis except the direct comparison of R with d′ (transformed into the familiarity estimates F) for which a two-way ANOVA was used to reveal the interaction effect.

Least-squares curve-fitting method, generation of ROC functions, R, d′

The best fitting ROC curve was obtained by using an Excel solver using a least-squares method with R and d′ as parameters that were also generated by the solver (Yonelinas et al. 1998). Briefly, the Excel solver uses a model for recognition memory that assumes that recognition is based on two distinct processes: recollection (R) and familiarity (F) and can be illustrated by the following equations:

graphic file with name 104equ1.jpg

and

graphic file with name 104equ2.jpg

in which d′ is the distance between the equal-variance Gaussian strength distributions for old and new items; ci, the response criterion at point i; and Φ, is the cumulative response function. To enable direct comparison between R and d′, we converted d′ into a familiarity estimate F, such that Fno deadline would be in the same range than Rno deadline (∼0.27). This was achieved by calculating the probability of a hit given a false alarm rate of 0.12.

z-Scores and z-ROC curves.

For each hit and false alarm rate, the z-scores corresponding to the area under the normal distribution (mean = 0; standard deviation = 1) were calculated, and these z-scores were fitted with a linear regression to plot the z-ROC curve.

Acknowledgments

We thank J. Frank for assistance with graphic designs. This work was supported by U.S. National Institute of Mental Health grants MH52090and MH71702. The authors declare that they have no competing financial interests.

Footnotes

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